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Vet. Res. 34 (2003) 689–716                                                                                                                         689
© INRA, EDP Sciences, 2003
DOI: 10.1051/vetres:2003030
                                                                                                                       Review article

                            Mastitis of dairy small ruminants

          Dominique BERGONIERa*, Renée DE CRÉMOUXb, Rachel RUPPc,
                   Gilles LAGRIFFOULd, Xavier BERTHELOTa

             a École
                  Nationale Vétérinaire, UMR 1225 INRA-ENVT Host-Pathogens Interactions,
                        23 chemin des Capelles, 31076 Toulouse Cedex 3, France
      b Institut de l’Élevage, Chambre d’Agriculture du Tarn, BP 89, 81003 Albi Cedex, France
                     c INRA-SAGA, BP 27, 31326 Castanet-Tolosan Cedex, France
d Comité National Brebis Laitières – Institut de l’Élevage, BP 27, 31326 Castanet-Tolosan Cedex, France



                                        (Received 25 April 2003, accepted 23 June 2003)



Abstract – Staphylococci are the main aetiological agents of small ruminants intramammary
infections (IMI), the more frequent isolates being S. aureus in clinical cases and coagulase negative
species in subclinical IMI. The clinical IMI, whose annual incidence is usually lower than 5%,
mainly occur at the beginning of machine milking and during the first third of lactation. These
features constitute small ruminant peculiarities compared to dairy cattle. Small ruminant mastitis is
generally a chronic and contagious infection: the primary sources are mammary and cutaneous
carriages, and spreading mainly occurs during milking. Somatic cell counts (SCC) represent a
valuable tool for prevalence assessment and screening, but predictive values are better in ewes than
in goats. Prevention is most often based on milking machine management, sanitation and annual
control, and milking technique optimisation. Elimination mainly relies on culling animals
exhibiting clinical, chronic and recurrent IMI, and on drying-off intramammary antibiotherapy; this
treatment allows a good efficacy and may be used selectively by targeting infected udders only.
Heritability values for lactation mean SCC scores are between 0.11 and 0.15. Effective inclusion of
ewe’s mastitis resistance in the breeding goal has recently been implemented in France following
experimental and large scale estimations of genetic parameters for SCC scores.

ewe / goat / mastitis / somatic cell count / epizootiology


                                                               Table of contents

1. Introduction...................................................................................................................................... 690
2. Aetiology ......................................................................................................................................... 691
   2.1. Clinical mastitis....................................................................................................................... 691
   2.2. Subclinical mastitis ................................................................................................................ 691
3. Descriptive epizootiology: recent knowledge.................................................................................. 692
   3.1. Incidence, prevalence and persistence .................................................................................... 692
        3.1.1. Clinical mastitis ........................................................................................................... 692
        3.1.2. Subclinical mastitis ...................................................................................................... 692




* Corresponding author: d.bergonier@envt.fr
690                                                           D. Bergonier et al.


     3.2. Effects of stage and number of lactation on the IMI incidence and prevalence ......................693
          3.2.1. Lactation stage..............................................................................................................693
          3.2.2. Lactation number (parity).............................................................................................694
4.   Analytical epizootiology ..................................................................................................................694
     4.1. Sources and associated factors.................................................................................................694
          4.1.1. Sources .........................................................................................................................694
          4.1.2. Factors associated to bacterial persistence ...................................................................695
     4.2. Factors of susceptibility ...........................................................................................................696
          4.2.1. Genetic factors: recent advances ..................................................................................696
          4.2.2. Environmental factors ..................................................................................................696
     4.3. Transmission ............................................................................................................................697
5.   Diagnosis: new developments in the cytological detection of mastitis ...........................................697
     5.1. Milk cell subpopulations..........................................................................................................697
     5.2. Lentiviral variation factors of somatic cell counts...................................................................699
     5.3. Non-pathological variation factors of somatic cell counts ......................................................699
     5.4. Recent advances in the practical use of individual somatic cell counts ..................................701
          5.4.1. Punctual approach (and single threshold).....................................................................701
          5.4.2. Dynamical approach and multiple thresholds ..............................................................702
6.   Treatment..........................................................................................................................................703
     6.1. Clinical mastitis .......................................................................................................................704
     6.2. Subclinical mastitis ..................................................................................................................704
     6.3. Risks associated with intramammary treatment ......................................................................705
          6.3.1. Clinical outbreaks .........................................................................................................705
          6.3.2. Residues........................................................................................................................705
7.   Disease control .................................................................................................................................705
     7.1. Vaccination ..............................................................................................................................705
     7.2. Preventive general management ..............................................................................................706
          7.2.1. Control of bacteriological sources................................................................................706
          7.2.2. Control of bacteriological transmission during milking...............................................706
          7.2.3. Limitation of receptivity and sensitivity.......................................................................707
     7.3. Genetic control.........................................................................................................................708
8.   Future prospects................................................................................................................................708



1. INTRODUCTION                                                                 short or absent suckling period, diversity of
                                                                                alimentation systems from zero-grazing to
   Intramammary infections (IMI) in dairy                                       traditional extensive husbandry, etc. Thus
small ruminants are mainly of bacterial ori-                                    control strategies are based upon the same
gin; this paper does not deal with lentiviral                                   principles, but vary to a certain extent. On
or mycoplasmal infections (see [15, 19]).                                       the contrary, important differences exist
Ovine and caprine IMI epizootiology and                                         regarding cow IMI, which first led to
control share numerous common points,                                           improving basic knowledge and more
but are different from some physiopatho-                                        recently to validating specific control pro-
logical points of view: in goats, there are                                     grammes.
shorter (or even no) dry period, more varied
variation factors of somatic cell counts                                           The importance of mastitis is mainly
(SCC), lentiviral mammary infection, higher                                     economic, hygienic (dairy products con-
‘stress’ susceptibility, etc. These also differ                                 sumers) and legal in Europe (E.U. Direc-
due to certain husbandry methods: in goats,                                     tives 46/92 and 71/94 defining the
generally lower kidding synchronisation, a                                      bacteriological quality of milk).
Mastitis of dairy small ruminants                            691


2. AETIOLOGY                                     nosa (peri partum period and sometimes
                                                 drying-off), and more rarely to Burkholde-
2.1. Clinical mastitis                           ria cepacia or Serratia marcescens ([13,
                                                 23, 76, 110, 111, 145], Bergonier et al.,
   In sporadic cases for sheep and goats,        unpublished results).
the high prevalence of Staphylococcus
aureus has often been reported. In a             2.2. Subclinical mastitis
decreasing order of frequency, isolates
belong to Coagulase Negative Staphyloco-             Figure 1 shows that CNS are the most
cci (CNS), which cannot be considered as         prevalent, ranging from 25 to 93 %, before
minor pathogens in small ruminants, Strep-       S. aureus (3 to 37 %) mainly isolated from
tococci, Enterobacteria, Arcanobacterium         infections that had become chronic (less
pyogenes, Corynebacteria, Pasteurellaceae,       severe ones). Among the CNS, S. epider-
Pseudomonas spp., etc. [5, 14, 80, 146,          midis then S. xylosus, S. chromogenes and
153].                                            S. simulans are the more frequently isolated
   Enzootic or epizootic outbreaks are due       in ewes. In goats, S. caprae is one of the
to S. aureus, then to S. uberis, S. agalac-      most prevalent species, followed by the
tiae, S. suis (mainly during lactation) or to    former ones. In addition, among the CNS,
opportunistic pathogens such as Aspergil-        S. epidermidis is generally associated with
lus fumigatus and Pseudomonas aerugi-            the highest average values of SCC both in




                                                                   Figure 1. The aetiology of
                                                                   ovine and caprine subclinical
                                                                   intramammary infections.
692                                   D. Bergonier et al.


ewes and goats, on the contrary to               two species, mammary pathology is the
S. caprae. Sixty to more than 80% of CNS         first cause of culling for sanitary reasons;
strains isolated from subclinical IMI            it is more frequent during the first 2–
produce evidence of alpha, delta or syner-       3 months of lactation [92].
gistic haemolysis. These haemolytic strains         The persistence of mammary symp-
induce significantly higher SCC than non-        tomatology after clinical cases during the
haemolytic ones. Leucotoxin production is        dry period is not well documented but prob-
absent or lower in CNS than in S. aureus.        ably high [131], above all in goat husbandry
In the latter species, caprine and ovine mas-    characterised by a shorter dry period (1 to
titis isolates are more leukotoxic than          3 months) than in that of the ewe (2 to
bovine ones. Listeria monocytogenes and          5 months). Culling of mastitic (even chronic)
Salmonella spp. IMI are very rare but            animals is highly recommended.
important; these organisms can cause
chronic and subclinical IMI [2, 8, 14, 17,
                                                 3.1.2. Subclinical mastitis
21, 28, 29, 38, 40, 68, 70, 75, 80, 109, 115,
129, 130, 143, 144].
                                                    The prevalence may be assessed, as in
                                                 dairy cattle, by the analysis of bulk milk
                                                 somatic cell counts (bSCC), which is the
3. DESCRIPTIVE EPIZOOTIOLOGY:
                                                 only easy and cheap way to estimate the
   RECENT KNOWLEDGE                              whole flock/herd mammary infectious sta-
                                                 tus (exhaustive individual SCC [iSCC] are
3.1. Incidence, prevalence                       rarely available). In several regions, bSCC
     and persistence                             are carried out every month (or more) in
                                                 every flock. Recent data are available
3.1.1. Clinical mastitis                         regarding the relationship between bSCC
                                                 annual mean or punctual values and the rate
   The incidence is usually lower than 5%        of presumed infected animals [73]. In
per year. In a low percentage of herds, the      ewes, the annual mean bSCC (weighted by
incidence is higher and may exceed 30–           the volumes) is closely linked (r2 = 0.845)
50% of the animals, causing mortality or         to the proportion of presumed ‘persistently
culling of up to 70% of the herd. S. aureus,     infected’ ewes, using the thresholds pro-
Streptococci or opportunistic pathogens          posed by Bergonier and Berthelot [14]. An
generally cause these outbreaks [32, 60,         increase of 100 000 cells per mL was asso-
69, 71].                                         ciated with a rise of estimated prevalence
   The persistence of individual clinical        of about 2.5% [73]. In Spanish flocks with
IMI during lactation depends on the techni-      250 000 and 1 million cells per mL, the
cal level, the flock size and the type of milk   prevalence was estimated to 16 and 35%
payment and valorisation (raw versus pas-        respectively, considering as infected an
teurised milk). It is rarely documented and      ewe with iSCC over 340 000 cells per mL
traditionally high, except for peracute cases    [120]. The bSCC values and their corre-
[20]. Mastitic animals are not often imme-       spondence with iSCC allow a good estima-
diately culled, and acute cases may become       tion of prevalence.
chronic for several months or more (1.5 to          In goats (Fig. 2), this relationship is
more than 30%). In ewe flocks, culling for       rather delicate to define, taking into account
IMI is increasing up to 7% of total causes       the incidence of lentiviral mastitis and the
in the Lacaune breed (Lagriffoul, unpub-         importance of non infectious variation fac-
lished results). In specialised goat herds,      tors of SCC. The influence of the kidding
18% of the animals culled or dead for dis-       season on the bSCC values has been
ease reasons experienced mastitis. In the        reported [52]. The dynamics of infections
Mastitis of dairy small ruminants                            693




Figure 2. Relation between annual geometric mean of bulk somatic cell counts and prevalence of
subclinical intramammary infections estimated by individual somatic cell counts in goats and ewe
herds/flocks ([73, 74], De Cremoux, unpublished results).


can also vary according to the flock’s struc-     caused by one pathogen with an average
ture and breeding management: percent-            shedding duration of three to four months
ages of primiparous goats or prolonged            at least (± 2.5 months). Two or three succes-
lactation goats, period and distribution of       sive and different infections also occurred
droppings, etc. [43]. Preliminary results are     frequently (Bergonier and Berthelot, unpub-
available from 155 French herds: annual           lished data).
geometric means of 750 000, 1 000 000 and             The persistence of subclinical IMI dur-
1 500 000 cells/mL corresponded respec-           ing the dry period is important to consider
tively to 30% (± 12%), 39% (± 8%), 51%            regarding the treatment strategies. An over-
(± 8%) of presumed infected goats [42, 43].       all self-cure rate of 35 to 67% and of 20 to
                                                  60% of halves was estimated respectively
   Table I presents the geometric means of        in the ewe [17, 51, 64] and goat [81, 98,
bSCC performed in various European                112, 114]. Thus, percentages of spontane-
areas (European programme FAIR CT 95-             ous cure during the dry period are generally
0881: ‘Strategies of in farm control of SCC       lower in goats. If the infection substitutions
in ewe’s and goat’s milk’).                       during the dry period are taken into
                                                  account, these percentages are lower.
   The persistence of subclinical IMI dur-
ing lactation is variable according to the
causative pathogen but is generally high,         3.2. Effects of stage and number
since Staphylococci represent the more fre-            of lactation on the IMI incidence
quent ones [132]. Subclinical IMI are in               and prevalence
general poorly detected and not eliminated
at least during lactation. In two monthly         3.2.1. Lactation stage
surveys concerning a total of 768 udder-
halves during entire lactations (eight               The incidence of clinical IMI does not
months) in six dairy flocks, 45 to 50% of         vary with the lactation stage in the same
infected halves exhibited a single IMI            way as in dairy cattle. A high incidence at
694                                    D. Bergonier et al.


Table I. Geometric means of bulk milk somatic cell counts in various areas of the ewe’s and goat’s
milk production (in thousands cells per mL) (Source: annual reports of the European programme
FAIR CT 95-0881: ‘Strategies of in farm control of Somatic Cell Counts in ewe’s and goat’s milk’).

Species        Areas of production     1995      1996    1997      1998   1999   2000    Global
                     (breed)
Ewes          Castilla-León (Churra)     –        –          783   866    916      –       863
               Castilla-La Mancha       758      660         776   741    602     691      708
                  (Manchega)
             Spanish Basque country      –       481         482   473     –       –       477
                     (Latxa)
               Roquefort (Lacaune)      713      599         680   657    647     586      647
                Pyrenees (Basco-        642      642         663   733    750     710      690
               béarnaise, Manech)
                 Sardinia (Sarda)      1561      1624    1566      1416   1457   1493     1509
Goats          Castilla-La Mancha      2187      1259    1380      1318   1023   1071     1148
             France (Alpine, Saanen)   1218      1111    1166      1226   1252   1309     1214
                 Sardinia (Sarda)      1595      1739    1516      1468   1483   1673     1575


drying-off or at parturition is observed in       3.2.2. Lactation number (parity)
very rare and specific cases (mycotic
agents or P. aeruginosa), in relation with           An increased prevalence related to parity
environmental contamination and/or poor           has been reported in ewes and goats [26, 56,
hygiene practices. On the contrary, the           80, 138]. Such descriptive data must be cau-
higher rates are observed at the beginning        tiously interpreted: the incidence is difficult
of machine milking and during the first           to differentiate from prevalence (chronicity
third of lactation. High incidence may be         or relapse), and older animals may be the
observed in dairy ewes during suckling or         more resistant ones.
suckling-milking periods [22, 76, 80].
   The variations of subclinical IMI inci-
dence according to the stage of lactation         4. ANALYTICAL EPIZOOTIOLOGY
should be assessed by systematic monthly
milk culturing of large numbers of healthy
udders. This kind of a study is very rare.        4.1. Sources and associated factors
Variations can be indirectly estimated
through SCC, allowing the analysis of large       4.1.1. Sources
data sets. They must be cautiously inter-
preted as infectious and milk dilution/con-          The primary sources are firstly animal
centration effects are added. In goats,           carriage and subclinical IMI. The main sig-
higher rates have been observed at the            nificant Staphylococci reservoirs are sub-
beginning of lactation [48, 128], but prev-       clinical and chronical IMI and teat
alence seems to increase throughout the           cutaneous infections (traumas, contagious
campaign (Fig. 3). In ewes, a high incidence      ecthyma). CNS and S. aureus can also be
was reported at the beginning of lactation        cultured from healthy teat skin (and other
[70, 80].                                         body sites or external orifices) ([27, 135],
Mastitis of dairy small ruminants                           695




Figure 3. Estimation of intramammary infection average prevalence throughout lactation in
155 French caprine herds [43]. Parturition took place in November and December. (Proportions of
presumed infected udders were estimated through individual somatic cell counts.)




Bergonier et al., unpublished results). Other    vival of this organism [27, 153]. P. aerugi-
bacteria also have animal primary sources:       nosa, S. marcescens can survive in teat
S. agalactiae, A. pyogenes, Mannheimia           dipping solutions or disinfected moist clus-
haemolytica, etc. The latter is carried in the   ters (Bergonier et al., unpublished results).
adults and suckling young’s mouth, naso-
pharynx and tonsils [134].                       4.1.2. Factors associated to bacterial
   Other primary sources are environmen-                persistence
tal: Enterobacteria and Enterococci are
found particularly in the litter, and Pseu-         Udder infection persistence is due to the
domonas spp. especially in water or a            lack of precocious IMI detection and sys-
humid environment. A. fumigatus and other        tematic application of control programmes:
fungi are isolated from mouldy forage, wet       teat antisepsis, antibiotherapy or culling.
bedding, litter, and air [110]. S. uberis and    In French dairy ewe recorded flocks
S. suis recognise mixed reservoirs: infected     (379 flocks of the Roquefort area), foremilk
animals, litter, and the environment.            inspection is exceptional, udder palpation
                                                 and California Mastitis Test (CMT) are
   The accessory sources are, for Staphy-        occasionally realised by 57 and 65% of the
lococci, housing, bedding, feedstuffs,           farmers; post-milking teat antisepsis and
air, insects, clusters, equipments, humans       drying-off antibiotherapy are performed in
(hands), other animals, etc. [3, 28, 139].       20 and 70% of the flocks, respectively
M. haemolytica can be found on the teat          (Lagriffoul, 2000, unpublished results).
skin of ewes soon after lambing [134] and        These percentages are high compared to
in the environment of diseased animals:          other dairy ewe areas and are increasing.
grass, water, straw bedding, etc. Colder,        In French goat herds, drying-off antibio-
wetter weather seems to prolong the sur-         therapy frequency increased from 62.7%
696                                     D. Bergonier et al.


in 1997 to 84.3% in 2000; teat antisepsis          mine SCS across lactation [123, 124]. The
progressed from 13.7 to 29.4% of the herds         results are in close agreement with dairy
[44].                                              cattle literature [125]. The genetic variabil-
    Extra-mammary bacterial persistence is         ity of SCS in dairy ewes appears sufficient
firstly due to hygienic or technical failures      to implement a selection. The evolution of
concerning the milking machine (over-used          the genetic determinism of SCS during lac-
liners, etc.). Very little literature is availa-   tation shows a moderate to strong increase
ble; incorrect machine disinfection (no            in heritability. The values are particularly
alternation acid-alkaline chlorinated water,       low on the first test days (0.01 to 0.04), then
too low water temperature) or the use of           between the beginning to the middle of the
rubber (vs. silicone) liners seems to be asso-     lactation, estimates range from 0.04–0.1 to
ciated with poorer tank milk bacterial             0.12–0.25 [9, 10, 83]. In dairy cattle, com-
counts in ewes.                                    parable studies reported a smaller increase
                                                   with days in milk, with higher values in the
   Secondly, high stocking density, partic-        first months of lactation [33, 36, 118].
ularly in intensively managed herds/flocks
or during the suckling period, may result in          Regarding relationships between udder
large air concentrations of total microor-         health and milk production traits, several
ganisms, mesophilic or coliform bacteria           studies indicate unfavourable positive
and staphylococci. These effects are prob-         genetic correlations between SCS and pro-
ably associated with incorrect ventilation         duction traits, ranging from 0.1 to 0.2 [9, 96,
and high relative humidity. The multiplica-        124], as in dairy cattle [125]. Additionally,
tion of various bacteria on the skin (and in       the risk of being predicted as subclinically
the litter) can be subsequently enhanced [2,       infected (according to French SCC thresh-
137, 139].                                         olds) is significantly increased in the high,
                                                   versus low, divergent lines selected on milk
                                                   production in the La Fage experimental
4.2. Factors of susceptibility                     flock [9]. On the contrary, some authors
                                                   found a favourable negative genetic corre-
4.2.1. Genetic factors: recent advances            lation between SCS and milk yield, ranging
                                                   from –0.35 to –0.11 [10, 49, 50, 83], con-
   Several studies on resistance to mastitis       cluding that selection for increased milk
have been recently based on SCC as an              yield might not result in an unfavourable
indirect way of measuring udder sanitary           response for SCC. Discrepancies between
status in dairy sheep (no literature data is       the results could be due to differences in
available in dairy goats).                         breeds, modelling and nature of the SCC data.
   Genetic parameters for SCC are calcu-
lated after logarithmic transformation of          4.2.2. Environmental factors
the values, i.e. somatic cell scores (SCS).
The results based on repeatability test day           Milking equipment and milking routine
models for SCS indicate variable heritabil-        are the main receptivity factors during lac-
ity estimates from 0.04 to 0.17 [9, 10, 49,        tation. In ewes, association between teat
63, 83]. Most studies based on larger data         injuries and mastitis has been reported [5].
sets for the Churra and Lacaune breeds             The limitation of udder massages and strip-
reported consistent heritability values            ping is associated with a significant positive
between 0.11 and 0.15 for the lactation            effect for primiparous goats: a decrease of
mean SCS [9, 50, 123, 124]. A high genetic         IMI and teat congestions. Over-milking
correlation between the first and second           limitation (respectively suppression) may
lactation (0.88–0.93) has been reported,           be associated with the reduction of hyper-
indicating that mostly the same genes deter-       keratoses (respectively reduction of minor
Mastitis of dairy small ruminants                            697


pathogen IMI prevalence), but data con-           5. DIAGNOSIS:
cerning over-milking are rather inconsist-           NEW DEVELOPMENTS
ent; it is probably better tolerated by healthy      IN THE CYTOLOGICAL
udders [44]. A vacuum level increase may             DETECTION OF MASTITIS
induce a rise of SCC without clinical IMI
[88, 140].                                          Clinical and bacteriological diagnosis
   Intramammary infusions at drying-off           will not be considered, as recent advances
or during lactation may cause teat duct cell      mainly concern detection of subclinical
damages.                                          IMI by SCC.
   The factors affecting sensitivity are not
very well known (very few data are availa-        5.1. Milk cell subpopulations
ble about udder immunity). In dairy ewes,
parenteral administration of vitamin E and            Small ruminant milk contains the same
selenium during the dry period can reduce         types of cells as cow’s milk, but important
SCC and increase the percentages of milk          differences exist between ewe and goat
neutrophils during the subsequent lactation       milk cells in subpopulation percentages
[102, 121]. Sensitivity may also be increased     and total counts (Tab. II).
by milk retention, due to a bad working               In bacteriologically negative ewe’s milk,
milking machine, under-milking, stressful         epithelial cells seem to be less than 2–3%
or painful milking and even udder morphol-        of somatic cells, polymorphonuclear neu-
ogy. Milk kinetics analysis allows to evi-        trophil leukocytes (PMNL) constitute 10–
dence too short milking times: 12 to 14% of       35%, macrophages 45–85% and lym-
under-milking (1023 kinetics) have been           phocytes 10–17%. These percentages do
observed in goats [24].                           not vary to a large extent with the lactation
                                                  stage, excluding the beginning of lactation
                                                  (particularly the colostral period) and the
4.3. Transmission                                 involutive period: in early involution secre-
                                                  tion, PMNL increase; they decline 21 days
   Spreading mainly occurs during milk-           after cessation of lactation [78]. These per-
ing. Udder massage and stripping induce           centages are close to those of cow’s milk
air intakes leading to impact. Cluster            (2–30% for PMNL for example); in both
removal by the milker may also induce             species, the macrophage is the major cell
                                                  type in bacteriologically negative milk [99,
impact, since it is often performed without
                                                  106, 108]. There is a high correlation in
previous vacuum cutting off (the automatic
                                                  ewes and cows between PMNL percent-
cluster removal is developing). Bacteria are      ages and SCC [59, 103].
also transported passively by liners. How-
ever, the IMI prevalences do not seem to be           On the contrary, in goats, several cyto-
significantly different between dairy (hand       logical peculiarities must be underlined for
or machine milked) and meat flocks. Trans-        their biological as well as operational (IMI
                                                  detection) interests. First of all, milk secre-
mission is also possible by “milk-robber”
                                                  tion in goats is apocrine [149, 150]: cyto-
lambs (buccal carriage) and may be impor-
                                                  plasmic particles are physiologically shed
tant for staphylococci, Pasteurellaceae,          into milk from the apical portion of secre-
parapox virus (contagious ecthyma), etc.          tory cells. Although most of them are anu-
   Penetration of the udder by organisms          cleated, some of these particles have been
is performed via the teat duct. In cases of       observed to contain nuclear fragments
systemic infections, haematogenous colo-          [107] and could contribute to a slight extent
nisation is frequent (lentivirosis, myco-         to the total cell count. Cytoplasmic particles
plasmosis, brucellosis, etc.).                    are similar in size to milk somatic cells.
698                                          D. Bergonier et al.


Table II. Distribution of leucocyte subpopulations in small ruminant milk.

Species Reference Year n         Milk type        Lactation (L.) Neutrophils Macrophages Lymphocytes
                                                      stage          %           %           %
Goats      [46]    1982 56      uninfected           early L.          45           35          20
                                  halves
                          4     uninfected            late L.          74           15           9
                                  halves
           [45]    1993 70       bulk tank                            87.3          9.9         2.8
          [122]    1993 200       halves          weeks 1–4 pp 45.8 to 52.5 19.6 to 27.2 12.9 to 14.1
                                  halves         weeks 28–31 pp 68.6 to 70.3 12.0 to 12.5    2.9 to 4.3
           [93]    1998 12        halves          weeks 2–3 pp          –           80           –
                                                   weeks 4–18          50           45           –
                                                  ³ 19 weeks pp        80            –           –
           [52]    1999 950       halves                –             40.9         35.6         0.7
          [151]    2002 237       halves             early L.          79            –          22
                         36       halves              late L.          78            –          22
Ewes       [55]    1985 84      uninfected           mid-L.        26.5 to 58.5      –           –
                                  halves
                         12     uninfected       early drying-off 69.7 to 85.8       –           –
                                  halves
           [59]    1985 91        halves             mid-L.         10 to 90      0 to 60     8 to 18
           [77]    1976 6         halves            dry udder           –           84           6
           [78]    1981 6         halves            colostrum       41 to 84      8 to 49     6 to 11
                          6       halves             mid-L.             –         83 to 86   10 to 17
           [99]    1994 –       uninfected          whole L.           30           60           8
                                  halves
          [100]    1996 640     uninfected          whole L.          34.9           –           –
                                  halves
                         50 infected halves         whole L.       52.1 to 82.2      –           –
          [101]    1996 10 healthy halves           whole L.          30.6         57.3         8.2
          [103]    2001 40      uninfected           mid and       31.1 to 52.6      –           –
                                  halves             late L.*
                              infected halves        mid and       65.9 to 77.6      –           –
                                                     late L.*
pp: postpartum. * No significant evolution according to the lactation stage.
Mastitis of dairy small ruminants                            699


Their average concentrations in milk is             In goats, there is a little more informa-
150 ´ 103/mL for goats and 15 ´ 103/mL for       tion concerning the relationship between
ewes [108]. Furthermore, numerous inves-         CAEV and SCC or the prevalence of sub-
tigators reported unexpected SCC increases       clinical IMI. A relationship between sero-
and high PMNL percentages (Tab. II):             logical status and bacterial IMI was
PMNL comprise the major cell type in milk        reported in herds with a high prevalence
from uninfected goats [108]. In normal late      of CAEV and IMI [62, 127, 129, 142].
lactation milk, they constitute 74–80% of        This was attributed to a selective immuno-
total cells. A significant increase has been     suppression due to altered macrophage
found in PMNL chemotactic activity dur-          function during CAEV infection. In serop-
ing this stage compared to early lactation       ositive goats, an increase of SCC was
and inverted evolution of mononuclear            mostly reported as far as bacteriologically
cells chemotactic activity. Differences          uninfected halves are concerned [82, 105,
between chemotactic cytokine profiles of         127, 130]. This could be related to the larger
mastitic and normal late-lactation-stage         number of macrophages in the milk of
milk suggest the existence of a physiologic      CAEV contaminated goats [82]. Neverthe-
regulation in the influx of PMNL into the        less, it was weak [82, 129] and lower than
milk. The authors suspected PMNL to serve        those due to bacterial infections. The effect
as physiological regulators in the early         of CAEV on SCC was not apparent when
phase of the involution process [93]. In         udder halves showed a persistent subclini-
early lactation also, goat milk generally        cal IMI. This failure of the inflammatory
contains a higher PMNL proportion than           response was interpreted as a reduction in
the others. It has been suggested that leuko-    the activity of macrophages caused by the
cyte migration could proceed at a faster rate    viral infection. Some cytokines, such as
than that into cow’s milk and might contrib-     chemotactic factors for neutrophils, and
ute to naturally higher SCC [107]. The           some mediators such as interleukin-8 could
hypothesis of different defense mecha-           be involved in this process [129].
nisms for the goat udder than for the bovine
udder has been considered [97]. Some             5.3. Non-pathological variation factors
authors suggest that in goats compared to             of somatic cell counts
dairy cattle, the low incidence of clinical
IMI might be related to the physiologically         The main variation factors for healthy
high SCC and PMNL percentage. This               udders are, in decreasing order of fre-
hypothesis is weakened by the comparison         quency, lactation stage, lactation number or
with the ewes situation: the same low clin-      within-day fluctuations, and milk fractions.
ical IMI incidence and, on the contrary to       The nature and importance of these factors
goats, the same range of somatic cell counts     have already been described [18, 60, 72,
and percentages as in the cow.                   108]. Briefly, in the ewe they are responsi-
                                                 ble for geometric mean variations ranging
5.2. Lentiviral variation factors                from 40 000 to 100 000 cells/mL, the mean
     of somatic cell counts                      iSCC values for uninfected ewe udders in
                                                 mid-lactation ranging from 100 000 to
   The mammary gland of the goat and             250 000 cells/mL [18, 58, 108, 123]. The
ewe is a target organ for lentiviral infec-      lactation stage is the first of these factors.
tions, but an additional difference between      Irrespectively of the infectious status, SCC
the two species is reported. In the ewe, no      values increase as the stage of lactation
clear evidence is available for influence of     progresses, above all in goats (Figs. 4 and 5):
Maedi-Visna infection on SCC at a large          average values during the first three months
scale [79].                                      are 200 ´ 103 cells/mL, and progressively
700                                      D. Bergonier et al.




            (b)




Figure 4. The effect of lactation stage on individual somatic cell counts according to the infectious
status of the mammary gland of ewes (a) (Rupp, unpublished results) and goats (b) [41, 94].




increase to more than 106 cells/mL during           udders, whose SCC values show less
the latter months [108]. In ewes, counts are        fluctuations than those of goats, the ‘flock-
higher during the first few weeks of lacta-         campaign’ effect appears to be the most
tion and decrease at the maximum milk               important [123].
production. Average SCC (and PMNL per-                 Minor or punctual SCC variation fac-
centages) are also affected by parity (Fig. 5)      tors may exist according to the manage-
[38, 41, 71, 122, 147]. For healthy ewe             ment of the flock/herd. In ewes, the number
Mastitis of dairy small ruminants                            701




Figure 5. Illustration of the lactation number (parity) effect on individual somatic cell counts
throughout the lactation of uninfected ewes [123] and goats [41]. Lac: lactation.


of suckling lambs, the suckling-milking           tion status among the indirect tests availa-
period management, the lambing month,             ble at the moment [14, 91].
and sudden dietary transitions are respon-
sible for mild variations, whose geometric
mean is generally lower than 20 000 cells/        5.4. Recent advances in the practical
mL [71, 72, 123]. In goats, vaccinations,              use of individual somatic cell counts
treatments, abrupt dietary modifications,
stress, etc. have been found to increase
SCC [82]. A significant SCC increase with         5.4.1. Punctual approach (and single
a simultaneous decrease of production has                threshold)
been observed during induced estrus. This
effect is accentuated in infected halves ([4,        This simple and quite early methodol-
91], Poutrel, unpublished data).                  ogy proposes the punctual or instantaneous
                                                  discrimination between ‘healthy’ and
   In conclusion, important differences           ‘infected’ udders, generally using a single
concerning differential and total counts,         threshold. Thresholds are sometimes pro-
lentiviral infection effect and non-patho-        posed for milk to be tested bacteriologi-
logical variation factors exist between           cally. The threshold determination is
dairy ewes and cows and, on the other             usually based on the comparison of iSCC
hand, goats. For the latter, cellular recruit-    of punctually infected and uninfected
ment is characterised by a more important         halves, or on the choice of the best compro-
number and diversity of factors, and by           mise between sensitivity and specificity.
greater inter-individual and temporal vari-       Briefly, an analysis of the available litera-
ations. The signification of goat milk cellu-     ture bring forth the differences on the tech-
larity fluctuations is not so far completely      nical and methodological levels [40]. In
understood. Nevertheless, bacterial IMI is        goats, the apocrine character of lacteal
the main variation factor of SCC, which           secretion implies specific coloration of
was found to be the best predictor of infec-      DNA in order to differentiate cytoplasmic
702                                   D. Bergonier et al.


particles from leukocytes [46, 152]. Large       dynamic character of infection and cellular
differences concerning the thresholds are        response. Cut-off recommendations have
also notable, even when considering stud-        moved towards the use of consecutive iSCC
ies using the fluoro-opto-electronic (FOE)       per lactation and the definition of two (or
method. The validity parameters (sensitiv-       three) thresholds within the same detection
ity, specificity, predictive values, etc.) of    systems. An important reason is that sta-
such detection methods are also highly var-      phylococcal IMI are characterised by
iable and consequently will not be reported.     dynamic fluctuations and consequently
                                                 cyclic milk shedding, potentially causing
   In ewes with the FOE method, the single       false-negative bacteriological results. ‘Inter-
thresholds proposed surprisingly range           mittent isolations’ have been reported [27,
from 200 000 to 1.5 million cells/mL; nev-       132]. This bacterial cyclicity is generally
ertheless the majority of them are below         inverted to PMNL one, since neutrophil
500 000 cells/mL [57, 58, 90, 95, 109, 119].     infiltrates usually eliminate most but not all
Some authors suggested using two thresh-         bacteria; SCC fluctuate according to the
olds to distinguish ‘healthy’ from ‘infected’    organisms number and viability [39, 116,
udders (140 000 and 340 000 cells/mL,            136, 148]. On the contrary, discordance
[120]) or ‘minor’ from ‘major’ pathogen          between some chronic IMI and SCC values
IMI (244 000 and 106 cells/mL, [144]).           is due to the important heterogeneity in
                                                 CNS field strain virulence. For example in
   In goats, for healthy halves, arithmetic      ewes, the SCC mean induced by S. lentus
means with the FOE method range from             is very close to that of uninfected halves
520 000 to 1.1 ´ 106 cells/mL [37, 41, 82,       [14].
113] and geometric means from 223 000 to
396 000 cells/mL [37, 41, 90]. The cut-off          Consequently, one should prefer to use
values range from 500 000 to 1.5 ´               detection systems defining a third class of
106 cells/mL [37, 67]. The studies and           ‘doubtful’ udders and the combination of
results differ depending on whether they         several successive SCC, as in dairy cattle,
consider the nature (‘minor’ versus ‘major’      rather than punctual approaches. A geo-
                                                 metric mean is sometimes employed, but
pathogens), intensity or persistence of IMI,
                                                 generally one or several criterions based on
and impact of non-infectious factors.
                                                 the number of SCC exceeding the thresh-
Among them, lactation stage has been pro-
                                                 olds are used. Methodologically, these
posed to be included in the definition of a
                                                 proposed standards originate from the
series of threshold values: according to cer-    comparison of monthly SCC throughout
tain authors, defining punctual standards        the lactation to the results of monthly bac-
for goat SCC is not possible without con-        teriological analysis of udder-halve milk
sidering lactation stage and probably parity     samples. In goats, since 2000, development
[60]. Using monthly SCC, a linear regres-        of udder health management programmes
sion allowed the determination of cut-off        in France is based on a synthesis of two
values from 556 000 cells/mL (90 days in         studies [11, 41] (Tab. III) (SCC standards
milk) to 1.2 ´ 106 cells/mL (305 days) [60].     are used for milk quality payment). The lat-
                                                 ter defined thresholds related to various
                                                 operational strategies, since the develop-
5.4.2. Dynamical approach and multiple
                                                 ment of a single criterion is difficult in
       thresholds                                goats. Four criterions are proposed depend-
                                                 ing on the nature of the infections, period of
   In addition to the necessity to take into     detection (early lactation, drying off) and
account these identified non-infectious var-     practices (preventive or curative) for con-
iation factors, other reasons explain that       trolling IMI. In ewes (Tab. III), it is also
studies have recently been focused on the        possible to use geometric means or numbers
Mastitis of dairy small ruminants                               703


Table III. Dynamic approaches for somatic cell count detection of subclinical mastitis.
Reference Year      Infection type      Criterion SCC N° Threshold         Test validity parameters (%)
                                                                          Sens. Spe. PPV NPV Eff.
Detection of infected goat halves
[128]       1998    All infections      Geometric     6       1 100       57.4   75.9 15.6    95.8 74.7
                                          mean
[65]        1990    All infections     No. of over             800        62.5   87.0 61.4    92.5 80.9
                                       counting: 2
Detection of infected goat udders
[41]        1995 Minor pathogens No. of over          6        750        82.6   60.9 77.5    68.2 73.1
                                 counting: 2
                   Major pathogens No. of over        6       1 750       61.3   80.2 16.5    97.0 79.2
                                   counting: 3
[11]        1998       S. aureus       No. of over   C1 +     3 000       81.8   95.3 42.9    99.2 94.7
                                       counting: 1    C2
                       S. aureus       No. of over C3 to      2 000       73.3   91.2 33.3    98.3 90.2
                                       counting: 3 Cn
                       S. aureus       No. of over C1 to      2 000       100.0 74.1 18.7 100.0 75.6
                                       counting: 2 Cn
                   All (primiparous) No. of over C1 to         600        90.9   85.7 90.9    85.7 88.9
                                     counting: 2 Cn
Detection of infected ewe udders
[16]
[14]
           1996a Short infection or No. of over
           2003     ‘doubtful’      counting: 3
                   Durable infection No. of over
                     or ‘positive’   counting: 2
                                                      7


                                                      7
                                                               500


                                                              1 000
                                                                      }   84.1   66.3    –      –   71.1



Sens.: sensitivity; Spe.: specificity; PPV and NPV: positive and negative predictive values; Eff.: effi-
ciency.
Thresholds: ´ 1000 cells/mL. SCC: Somatic Cell Counts. SCC N°: number of SCC.


of over counting, with thresholds and valid-           6. TREATMENT
ity parameters close to those of the dairy
cow [14, 16]. In both species, this kind of               In small ruminant field conditions, clin-
screening methodology can be adapted to                ical and subclinical IMI treatments must be
operational purposes (detection for culling,           distinguished, the average treatment cost
drying-off treatment, etc.) and sometimes              per animal being high in comparison with
to IMI prevalence assessment [90]. Usu-                the culling value and the expected recov-
ally, in field conditions, a few iSCC values           ery. In (per)acute clinical cases, the first
are available per lactation. In these cases,           purpose is to save the animal’s life and,
priority can be given to sensitivity, specif-          possibly, to save the diseased halves. In
icity, or predictive values in order to                some areas, antibiotherapy is more and
compensate for the decrease of overall effi-           more used at drying-off, particularly for
ciency.                                                milk cellular quality control [22, 114].
704                                   D. Bergonier et al.


   Most of the published papers report           ing bacteriological cure or prevention. The
clinical observations and/or recommenda-         overall cure rate ranges from 65 to 95.8%
tions adapted from results obtained in the       in the ewe [1, 35, 64, 86, 87] and from 50
cow; control-case studies are rare. Moreo-       to 92.5% in the goat, whose dry period is
ver, due to the general lack of specifically     shorter [7, 54, 89, 112, 114]. The efficacy
designed treatments for small ruminants,         is better for CNS than for S. aureus infec-
those for cattle are used (very few treat-       tions. These cure rates are higher than
ments are labelled for ewe and goat).            spontaneous cure rates (see Sect. 3.1.2.).
                                                     The preventive interest remains to be
6.1. Clinical mastitis
                                                 discussed, particularly in ewes, considering
    No results from a controlled trial are       the length of the dry period. Most bacteria
available on the efficacy (i.e. bacteriologi-    isolated from colostrum are not isolated
cal and clinical cure) of parenteral or          later in lactation (Berthelot, unpublished
intramammary antibiotherapy. A clinical          results). The new subclinical IMI rate at
study about tilmicosin treatment of ovine        lambing or kidding is therefore difficult to
staphylococcal IMI and mammary derma-            estimate (two successive bacteriological
titis recently reported a complete symp-         examinations are necessary). This rate is
tomatology decrease five days after a single     probably low, between 5 and 20%; very
dose (10 mg/kg); this treatment seems to         large data sets are therefore statistically
also have induced a cessation of milk shed-      needed to identify a possible positive pre-
ding from days 5 to 7. S. aureus and CNS         ventive effect of the drying-off treatment
showed greater in vitro susceptibility to        [1, 7, 17, 35, 87, 89].
tilmicosin than to various other antibiotics         Different treatment strategies are per-
[104]. Pharmacokinetics of various antibi-       formed regarding the target for antibiother-
otics have been studied after parenteral         apy. Additionally to the dry period length in
administration in the ewe and goat. Thera-       ewes, three other small ruminant peculiar-
peutical schemes have been proposed but          ities should be taken into account: the large
the efficacy has not been published so           herd size, the production cycle synchroni-
far: tobramycin (25 mg/kg) or apramycin          sation inducing a collective drying-off, and
(20 mg/kg) twice a day by intravenous            from a pathological point of view, the low
route; enrofloxacin (5 mg/kg) or norfloxacin     drying-off and peri partum IMI incidences.
(10 mg/kg) once a day by the intramuscular       Consequently, a selective drying-off ther-
route; tiamulin (25 mg/kg) twice a day by        apy (concerning the infected udders only)
the intramuscular route; florfenicol (20 to      may be preferred to a systematic one. The
25 mg/kg) twice a day by the intravenous or      limitation of the number of treatments
intramuscular route [155]. Under field con-      allows an easier implementation for a lower
ditions, beta-lactamines and macrolides are      cost and, overall, reduces the utilisation of
still widely used via the intramuscular route,
                                                 antibiotics and the risk of ‘iatrogenic’ udder
as recommended in former studies [154].
                                                 contamination [22, 54]. Udder examination
    As in cattle, complementary treatments       and iSCC or CMT are helpful to select the
may be implemented in the severe cases           ewes and goats requiring an antibiotic treat-
[14, 47]. The economic interest of these         ment. Drying-off antibiotherapy is gener-
treatments and also of new antimicrobial         ally performed once a year for the ‘whole’
drugs (fluoroquinolones) use remains to          flock, but early dried females (including
evaluated.                                       subclinical IMI) mostly remain untreated
                                                 [22]. For these females, antibiotherapy
6.2. Subclinical mastitis                        must not be implemented at this time by the
  The efficacy of drying-off intramam-           intramammary route since the teat duct is
mary antibiotherapy depends on consider-         sealed by a keratin plug; the parenteral route
Mastitis of dairy small ruminants                             705


is the only usable one. An elegant possibil-        During lactation, the infusion (three
ity is to perform two (or three) successive      syringes per udder-half at 12 h intervals) of
sessions of intramammary infusion accord-        a cattle-labelled formulation containing
ing to the respective lactation durations.       amoxicillin, clavulanic acid and pred-
    The intramuscular antibiotherapy (dry-       nisolone led to the detection of residues up
ing-off) would be an interesting route, par-     to 136 h in the ewe and 112 h in the goat
ticularly in large flocks, because it allows     after the last infusion [30, 31]. In a similar
an easier implementation and a reduction         study, cloxacillin residues were detected in
of the ‘iatrogenic’ risk of udder contamina-     goat’s milk up to 156 h after the last infusion
tion [155]. Nevertheless there is a lack of      [61]. These results justify the 7-days with-
published controlled trials. According to        drawal period prescribed by the European
field observations, two successive injec-        regulation after an out-of-label intramam-
tions at drying-off are needed to possibly       mary treatment in lactating small rumi-
obtain a significantly higher cure rate than     nants.
that of the untreated animals.                       After drying-off treatments of dairy
                                                 ewes with a cattle-labelled formulation
6.3. Risks associated with                       containing penicillin (300 000 IU), nafcil-
     intramammary treatment                      lin (respectively 100 and 109.2 mg) and
                                                 dihydrostreptomycin (respectively 100 and
6.3.1. Clinical outbreaks                        125 mg), residues were detected at lambing
                                                 in four (respectively five) ewes out of 190
   The development of drying-off intramam-       (respectively 25) and no more after three
mary antibiotherapy has been associated          (respectively 5) days [35, 84]. In goats
in sheep and goats with a few outbreaks          receiving the same formulation, residues
of (per)acute to chronic clinical mastitis       were found at kidding in some females
caused by opportunistic pathogens, espe-         whose dry period had been shorter than two
cially P. aeruginosa (at the peri-partum         months; no more residues were detected
period and sometimes at the beginning of         after seven days [85]. These results confirm
dry period) or A. fumigatus (at the peri-par-    previous data [54], who found residues
tum period) [13, 66, 76, 110, 111, 117]. In      in only 1 out of 34 treated goats after a
most cases, the hygiene precautions had not      107-day dry period.
been strictly respected at the time of imple-        Considering the dry period durations, it
mentation: teat-end disinfection, partial        can be assumed that the risk of residues in
and atraumatic introduction of the cannula,      milk is virtually null at lambing and, a for-
infusion of a complete syringe in each           tiori, at the first milk delivery after a one to
udder-half, teat antisepsis. Certain specific    two-month nursing period. On the contrary,
risk factors possibly existing at the time of    in the goat, the risk at kidding is present,
drying-off are now identified: liner contam-     particularly in cases of a shortened dry
ination originating from P. aeruginosa           period (shorter than two months); in the lat-
multiplication in machine residual water,        ter conditions, a 14-day withdrawal period
use of wet bedding or mouldy forage con-         is justified, as recommended in the cow.
taminated by A. fumigatus, etc. (Bergonier
and Berthelot, unpublished results).
                                                 7. DISEASE CONTROL
6.3.2. Residues
                                                 7.1. Vaccination
   The risk of antibiotic residues in milk
after intramammary treatments is poorly             No literature relative to recent advances
documented.                                      in IMI vaccination is available since the
706                                   D. Bergonier et al.


publication of a recent review [14]. Briefly,    tions regarding the pen and the stocking
regarding S. aureus, vaccine preparations        density.
based on bacterial cell extracts, capsular          The control of environmental sources
polysaccharides and/or toxoids, products of      first consists in applying the pen recom-
virulence regulation genes, adhesins, etc.       mendations for its conception, maintenance
have been proposed to prevent murine or          and stocking density (primary sources).
ruminant IMI. Attempts at immunisation           The pen management plays a key role in
with these preparations give generally           controlling environmental bacteria IMI,
insufficient results. In ewes, a liposome-       and indirectly helps to reduce staphylococ-
immunopotentiated exopolysaccharide vac-         cal pressure through controlling density
cine gave promising results [6]. Inactivated     and air humidity. These factors are likely to
vaccines and autovaccines are commer-            enhance air and cutaneous staphylococcal
cially available and widely used for ewes        concentrations. Stocking density may rep-
and goats in several countries. Information      resent a critical factor in housing; too small
about their efficacy in large scale controlled   space allocations may adversely affect per-
trials would be required.                        formances and health [137, 139]. For envi-
                                                 ronmental pathogens, the greatest care
7.2. Preventive general management               should be taken in the control of ambient
                                                 hygiene, especially through efficient litter
7.2.1. Control of bacteriological sources        management and ventilation systems [2].
                                                 This is of important concern in intensive
                                                 production systems, particularly in goats.
    The control of animal sources first tar-
gets intra-mammary carriage (primary                Secondly, the liners must be replaced
sources). This is mainly performed by dry-       every year for rubber ones, every two years
ing-off treatment of subclinical and mild        for silicone ones. The milking machine
chronic IMI and by culling the animals           (liners, clusters, pipelines, etc.) must be
who experienced acute or severe chronic          cleaned disinfected twice a day with drink-
IMI: udder asymmetry, diffuse hardness,          ing water and following a validated proce-
abscesses, etc. (abscesses must be differen-     dure (accessory sources).
tiated from cysts, generally located in
declivitous position sagital and close to the    7.2.2. Control of bacteriological
cisterns) [131]. After drying-off antibio-              transmission during milking
therapy, those animals still presenting
chronic signs at the beginning of the subse-        The milking technique represents a crit-
quent lactation should be culled.                ical point for IMI control, but the specific
    Mammary cutaneous carriage might be          risk factors associated to each time of the
controlled by pre-milking teat dipping; this     milking routine – and the milking equip-
measure is generally not used, due to herd       ment – have not been completely character-
sizes and milking routines, and probably to      ised. Over- and under-milking and every
the low incidence of bulk milk flora prob-       factor leading to impact (brutal and pro-
lems. In cases of staphylococcal dermatitis      longed stripping, cluster removal without
or contagious ecthyma, udder antisepsis,         vacuum cutting off) must be avoided.
isolation of affected animals and their             Some authors underlined that preventive
lambs, and sometimes antibiotherapy should       practices, including milking techniques,
be performed. The suckling lamb’s mouth          were required to provide an effective
and naso-pharynx carriage is important for       decrease of IMI rates [44]. Minimising air
staphylococci and M. haemolytica [3]. Its        inlets contributed to significant improvement
limitation relies on several other factors       in udder health status as far as minor path-
including the application of recommenda-         ogens presumed infections were concerned.
Mastitis of dairy small ruminants                          707


Minimising mammary massage, machine              7.2.3. Limitation of receptivity
stripping and avoiding the removal of extra-            and sensitivity
milk reattaching the teat cups is recom-
mended, particularly for primiparous females.       The non genetic control of udder recep-
The effect of milking techniques on bSCC         tivity is in particular based upon the reduc-
were only significant at the end of the          tion of teat lesions and pain caused by
lactation (the middle or long-term effect).      inadequate settings of the milking machine.
                                                    A survey on standards for small rumi-
    Post-milking teat antisepsis seems to        nants milking installations used in different
allow a 30 to 40% decrease of new IMI in         countries showed differences in ewes and
the goat. The reduction is more important at     goat husbandry leading to differences in
the beginning of lactation, when spontane-       requirements for milking equipment [24].
ous incidence is higher [12, 126]. The pos-      Effective reserve, vacuum pump capacity
itive effect on bSCC is also significant at      and pulsation characteristics are especially
the beginning of lactation [44]. Goat SCC        in question. The lack of available knowl-
analysis evidenced a decrease of primipa-        edge prevents from taking into account
rous early IMI and IMI recurrences [40]. In      specific characteristics of species and
another trial using iSCC but no bacteriol-       breeds in construction and installations of
ogy for the efficacy assessment, no differ-      milking machines. Annual checking and
ence was found between the dipped (nisin)        regular maintenance of milking machines
and undipped groups [114]. In dairy ewes         constitute basic measures insufficiently
also, teat-dipping or spraying is an efficient   applied since only 40 to 60% of the total
tool for reducing IMI incidence, above all       number of machines are checked annually.
in high prevalence situations (Berthelot         Mostly, the purpose of the investigations
et al., unpublished results). This preventive    was to study the influence of machine
measure is not frequently used, but could        parameters on milking efficiency [53, 141].
be implemented for a limited duration, dur-         Quantitative recommendations for small
ing the period at risk (the suckling-milking     ruminant milking installations were recently
period or the beginning of milking after         explored [25], with references to specific
weaning) or for controlling a mastitis or        equipments such as non conventional clus-
teat dermatitis outbreak. Its precise effec-     ters, references to specificity of milking
tiveness according to the antiseptic mole-       practices (attachment rates for example)
cules and to the different prevalence            and to typical lactation curves recorded in
conditions remains to be evaluated in small      various species and breeds. These recom-
ruminants, mainly in the ewe.                    mendations will evolve during the next
                                                 years and favour the development of relia-
   Implementing a milking order consists         ble analysis of machine milking impact on
in milking primiparous and/or healthy            teat duct health.
females first. In France, this heavy tech-          The control of udder sensitivity should
nique seems to be more frequent in goats         be based on dietary recommendations: lim-
than in ewes [44]. Its development may           itation of sudden transitions or lack of bal-
be associated with other advantages in           ance. On the contrary, milk retention must
goats regarding CAEV control, alimenta-          be reduced through adaptation of the equip-
tion or reproduction. Implementing a milk-       ment to animal yield, teat size and flock
ing order has been shown to be associated        size [53]: vacuum pump capacity, vacuum
with a decrease of (1) presumed major            reserve, claws volume and position with
pathogen associated IMI in primiparous           regards to the liners. Automatic cluster
goats, and (2) presumed minor pathogen           removal systems, when they exist, must be
associated IMI in multiparous goats [44].        carefully set.
708                                   D. Bergonier et al.


7.3. Genetic control                                The improvement of diagnosis would
                                                 also need, especially in small ruminants, the
    The genetic basis of susceptibility to IMI   development of rapid animal-side tests. The
has been established (moderate heritabili-       available tools are of limited interest: the
ties and QTL for SCC). Effective inclusion       foremilk visual examination and the Cali-
of mastitis resistance in the breeding goal of   fornia Mastitis Test can not be regularly and
Lacaune breed, based upon SCC, has been          systematically applied to large herds, and
recently implemented in France [124].            the on-line electrical conductivity measure-
Accordingly, breeders can choose their           ment needs efficiency improvement and
reproducer rams on mastitis resistance in        technical adaptations to small ruminant
addition to production traits (milk yield, fat   milking machines.
and protein contents) and PrP genotype              The assessment of bacteriological cure
(scrapie-resistant genotype). Improvement        and new infection rates during the dry
of resistance to mastitis by selection, how-     period, with or without antibiotic treatment
ever, is a long-term process and only par-       at drying-off, require additional informa-
tially efficient. Therefore, proper sanitary     tion in order to define and accurately choose
management remains the main clue to mas-         the differential treatment strategies. Con-
titis control.                                   trolled trials are needed to better determine
                                                 the bacteriological cure after drying-off
                                                 intramammary or parenteral (two succes-
8. FUTURE PROSPECTS                              sive injections) antibiotherapy, according
                                                 to the herd effects (main pathogens, infec-
   To control small ruminant mastitis,           tions length). They will also provide infor-
future research should concern the follow-       mation about the new infection rates at
ing fields, dealing with applied or basic        lambing/kidding, in order to rationalise the
research.                                        choice between systematic and selective
   The improvement of diagnosis, particu-        treatments and to assess the potential inter-
larly IMI cytological detection in goats.        est of teat sealers. Internal teat sealers are
Future research in this field should attempt     presumably less interesting in small rumi-
to determine the exact impact on total and       nants than in dairy cattle: the intramam-
differential counts of CAEV, herd manage-        mary implementation is not easier than
ment factors (dietary or medical stresses,       conventional treatments particularly for
etc.) and physiological factors (lactation       large flocks/herds, and the incidence of new
stage, estrus, etc.). Non infectious varia-      IMI during the dry period is lower.
tion factors of SCC are unique in the case          The assessment of preventive measures
of goats in comparison with ewes and             would be of particular interest regarding the
cows; the inflammatory and immune proc-          key-procedure in small ruminant IMI con-
esses of the caprine udder are not com-          trol: the milking machine management and
pletely understood. This point must be           the milking technique. Progress concerning
underlined since SCC are the only large          the former was published last year through
scale available screening tests to be used       quantitative recommendations for small
for control programmes, and since maxi-          ruminant milking machine installations
mum levels are held as standards by the          [25]. In the field, these recommendations
dairy industry or health officials. Progress     and the basic measures are insufficiently
in this field could be achieved by charac-       known and applied, and very different
terising bacteriologically negative halves       quantitative values are observed (particu-
with high and low SCC, at different lacta-       larly for pulsation rates). Moreover, addi-
tion stages, from cytological, biochemical       tional work is needed to clearly identify the
and histopathological points of view.            possible adverse effects of the equipment
Mastitis of dairy small ruminants                                     709


and milking routines on the receptivity of           [5] Ameh J.A., Tari I.S., Observations on the
the mammary gland and on the spreading of                prevalence of caprine mastitis in relation to
                                                         predisposing factors in Maiduguri, Small
organisms.                                               Rumin. Res. 35 (1999) 1–5.
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                                                         staphylococcal vaccine, Vaccine 12 (1994)
main causative agent of acute and peracute               243–249.
IMI. Immunity of the ovine and caprine
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                                                         Conference of the New-Zealand Society of
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titulo

  • 1. Vet. Res. 34 (2003) 689–716 689 © INRA, EDP Sciences, 2003 DOI: 10.1051/vetres:2003030 Review article Mastitis of dairy small ruminants Dominique BERGONIERa*, Renée DE CRÉMOUXb, Rachel RUPPc, Gilles LAGRIFFOULd, Xavier BERTHELOTa a École Nationale Vétérinaire, UMR 1225 INRA-ENVT Host-Pathogens Interactions, 23 chemin des Capelles, 31076 Toulouse Cedex 3, France b Institut de l’Élevage, Chambre d’Agriculture du Tarn, BP 89, 81003 Albi Cedex, France c INRA-SAGA, BP 27, 31326 Castanet-Tolosan Cedex, France d Comité National Brebis Laitières – Institut de l’Élevage, BP 27, 31326 Castanet-Tolosan Cedex, France (Received 25 April 2003, accepted 23 June 2003) Abstract – Staphylococci are the main aetiological agents of small ruminants intramammary infections (IMI), the more frequent isolates being S. aureus in clinical cases and coagulase negative species in subclinical IMI. The clinical IMI, whose annual incidence is usually lower than 5%, mainly occur at the beginning of machine milking and during the first third of lactation. These features constitute small ruminant peculiarities compared to dairy cattle. Small ruminant mastitis is generally a chronic and contagious infection: the primary sources are mammary and cutaneous carriages, and spreading mainly occurs during milking. Somatic cell counts (SCC) represent a valuable tool for prevalence assessment and screening, but predictive values are better in ewes than in goats. Prevention is most often based on milking machine management, sanitation and annual control, and milking technique optimisation. Elimination mainly relies on culling animals exhibiting clinical, chronic and recurrent IMI, and on drying-off intramammary antibiotherapy; this treatment allows a good efficacy and may be used selectively by targeting infected udders only. Heritability values for lactation mean SCC scores are between 0.11 and 0.15. Effective inclusion of ewe’s mastitis resistance in the breeding goal has recently been implemented in France following experimental and large scale estimations of genetic parameters for SCC scores. ewe / goat / mastitis / somatic cell count / epizootiology Table of contents 1. Introduction...................................................................................................................................... 690 2. Aetiology ......................................................................................................................................... 691 2.1. Clinical mastitis....................................................................................................................... 691 2.2. Subclinical mastitis ................................................................................................................ 691 3. Descriptive epizootiology: recent knowledge.................................................................................. 692 3.1. Incidence, prevalence and persistence .................................................................................... 692 3.1.1. Clinical mastitis ........................................................................................................... 692 3.1.2. Subclinical mastitis ...................................................................................................... 692 * Corresponding author: d.bergonier@envt.fr
  • 2. 690 D. Bergonier et al. 3.2. Effects of stage and number of lactation on the IMI incidence and prevalence ......................693 3.2.1. Lactation stage..............................................................................................................693 3.2.2. Lactation number (parity).............................................................................................694 4. Analytical epizootiology ..................................................................................................................694 4.1. Sources and associated factors.................................................................................................694 4.1.1. Sources .........................................................................................................................694 4.1.2. Factors associated to bacterial persistence ...................................................................695 4.2. Factors of susceptibility ...........................................................................................................696 4.2.1. Genetic factors: recent advances ..................................................................................696 4.2.2. Environmental factors ..................................................................................................696 4.3. Transmission ............................................................................................................................697 5. Diagnosis: new developments in the cytological detection of mastitis ...........................................697 5.1. Milk cell subpopulations..........................................................................................................697 5.2. Lentiviral variation factors of somatic cell counts...................................................................699 5.3. Non-pathological variation factors of somatic cell counts ......................................................699 5.4. Recent advances in the practical use of individual somatic cell counts ..................................701 5.4.1. Punctual approach (and single threshold).....................................................................701 5.4.2. Dynamical approach and multiple thresholds ..............................................................702 6. Treatment..........................................................................................................................................703 6.1. Clinical mastitis .......................................................................................................................704 6.2. Subclinical mastitis ..................................................................................................................704 6.3. Risks associated with intramammary treatment ......................................................................705 6.3.1. Clinical outbreaks .........................................................................................................705 6.3.2. Residues........................................................................................................................705 7. Disease control .................................................................................................................................705 7.1. Vaccination ..............................................................................................................................705 7.2. Preventive general management ..............................................................................................706 7.2.1. Control of bacteriological sources................................................................................706 7.2.2. Control of bacteriological transmission during milking...............................................706 7.2.3. Limitation of receptivity and sensitivity.......................................................................707 7.3. Genetic control.........................................................................................................................708 8. Future prospects................................................................................................................................708 1. INTRODUCTION short or absent suckling period, diversity of alimentation systems from zero-grazing to Intramammary infections (IMI) in dairy traditional extensive husbandry, etc. Thus small ruminants are mainly of bacterial ori- control strategies are based upon the same gin; this paper does not deal with lentiviral principles, but vary to a certain extent. On or mycoplasmal infections (see [15, 19]). the contrary, important differences exist Ovine and caprine IMI epizootiology and regarding cow IMI, which first led to control share numerous common points, improving basic knowledge and more but are different from some physiopatho- recently to validating specific control pro- logical points of view: in goats, there are grammes. shorter (or even no) dry period, more varied variation factors of somatic cell counts The importance of mastitis is mainly (SCC), lentiviral mammary infection, higher economic, hygienic (dairy products con- ‘stress’ susceptibility, etc. These also differ sumers) and legal in Europe (E.U. Direc- due to certain husbandry methods: in goats, tives 46/92 and 71/94 defining the generally lower kidding synchronisation, a bacteriological quality of milk).
  • 3. Mastitis of dairy small ruminants 691 2. AETIOLOGY nosa (peri partum period and sometimes drying-off), and more rarely to Burkholde- 2.1. Clinical mastitis ria cepacia or Serratia marcescens ([13, 23, 76, 110, 111, 145], Bergonier et al., In sporadic cases for sheep and goats, unpublished results). the high prevalence of Staphylococcus aureus has often been reported. In a 2.2. Subclinical mastitis decreasing order of frequency, isolates belong to Coagulase Negative Staphyloco- Figure 1 shows that CNS are the most cci (CNS), which cannot be considered as prevalent, ranging from 25 to 93 %, before minor pathogens in small ruminants, Strep- S. aureus (3 to 37 %) mainly isolated from tococci, Enterobacteria, Arcanobacterium infections that had become chronic (less pyogenes, Corynebacteria, Pasteurellaceae, severe ones). Among the CNS, S. epider- Pseudomonas spp., etc. [5, 14, 80, 146, midis then S. xylosus, S. chromogenes and 153]. S. simulans are the more frequently isolated Enzootic or epizootic outbreaks are due in ewes. In goats, S. caprae is one of the to S. aureus, then to S. uberis, S. agalac- most prevalent species, followed by the tiae, S. suis (mainly during lactation) or to former ones. In addition, among the CNS, opportunistic pathogens such as Aspergil- S. epidermidis is generally associated with lus fumigatus and Pseudomonas aerugi- the highest average values of SCC both in Figure 1. The aetiology of ovine and caprine subclinical intramammary infections.
  • 4. 692 D. Bergonier et al. ewes and goats, on the contrary to two species, mammary pathology is the S. caprae. Sixty to more than 80% of CNS first cause of culling for sanitary reasons; strains isolated from subclinical IMI it is more frequent during the first 2– produce evidence of alpha, delta or syner- 3 months of lactation [92]. gistic haemolysis. These haemolytic strains The persistence of mammary symp- induce significantly higher SCC than non- tomatology after clinical cases during the haemolytic ones. Leucotoxin production is dry period is not well documented but prob- absent or lower in CNS than in S. aureus. ably high [131], above all in goat husbandry In the latter species, caprine and ovine mas- characterised by a shorter dry period (1 to titis isolates are more leukotoxic than 3 months) than in that of the ewe (2 to bovine ones. Listeria monocytogenes and 5 months). Culling of mastitic (even chronic) Salmonella spp. IMI are very rare but animals is highly recommended. important; these organisms can cause chronic and subclinical IMI [2, 8, 14, 17, 3.1.2. Subclinical mastitis 21, 28, 29, 38, 40, 68, 70, 75, 80, 109, 115, 129, 130, 143, 144]. The prevalence may be assessed, as in dairy cattle, by the analysis of bulk milk somatic cell counts (bSCC), which is the 3. DESCRIPTIVE EPIZOOTIOLOGY: only easy and cheap way to estimate the RECENT KNOWLEDGE whole flock/herd mammary infectious sta- tus (exhaustive individual SCC [iSCC] are 3.1. Incidence, prevalence rarely available). In several regions, bSCC and persistence are carried out every month (or more) in every flock. Recent data are available 3.1.1. Clinical mastitis regarding the relationship between bSCC annual mean or punctual values and the rate The incidence is usually lower than 5% of presumed infected animals [73]. In per year. In a low percentage of herds, the ewes, the annual mean bSCC (weighted by incidence is higher and may exceed 30– the volumes) is closely linked (r2 = 0.845) 50% of the animals, causing mortality or to the proportion of presumed ‘persistently culling of up to 70% of the herd. S. aureus, infected’ ewes, using the thresholds pro- Streptococci or opportunistic pathogens posed by Bergonier and Berthelot [14]. An generally cause these outbreaks [32, 60, increase of 100 000 cells per mL was asso- 69, 71]. ciated with a rise of estimated prevalence The persistence of individual clinical of about 2.5% [73]. In Spanish flocks with IMI during lactation depends on the techni- 250 000 and 1 million cells per mL, the cal level, the flock size and the type of milk prevalence was estimated to 16 and 35% payment and valorisation (raw versus pas- respectively, considering as infected an teurised milk). It is rarely documented and ewe with iSCC over 340 000 cells per mL traditionally high, except for peracute cases [120]. The bSCC values and their corre- [20]. Mastitic animals are not often imme- spondence with iSCC allow a good estima- diately culled, and acute cases may become tion of prevalence. chronic for several months or more (1.5 to In goats (Fig. 2), this relationship is more than 30%). In ewe flocks, culling for rather delicate to define, taking into account IMI is increasing up to 7% of total causes the incidence of lentiviral mastitis and the in the Lacaune breed (Lagriffoul, unpub- importance of non infectious variation fac- lished results). In specialised goat herds, tors of SCC. The influence of the kidding 18% of the animals culled or dead for dis- season on the bSCC values has been ease reasons experienced mastitis. In the reported [52]. The dynamics of infections
  • 5. Mastitis of dairy small ruminants 693 Figure 2. Relation between annual geometric mean of bulk somatic cell counts and prevalence of subclinical intramammary infections estimated by individual somatic cell counts in goats and ewe herds/flocks ([73, 74], De Cremoux, unpublished results). can also vary according to the flock’s struc- caused by one pathogen with an average ture and breeding management: percent- shedding duration of three to four months ages of primiparous goats or prolonged at least (± 2.5 months). Two or three succes- lactation goats, period and distribution of sive and different infections also occurred droppings, etc. [43]. Preliminary results are frequently (Bergonier and Berthelot, unpub- available from 155 French herds: annual lished data). geometric means of 750 000, 1 000 000 and The persistence of subclinical IMI dur- 1 500 000 cells/mL corresponded respec- ing the dry period is important to consider tively to 30% (± 12%), 39% (± 8%), 51% regarding the treatment strategies. An over- (± 8%) of presumed infected goats [42, 43]. all self-cure rate of 35 to 67% and of 20 to 60% of halves was estimated respectively Table I presents the geometric means of in the ewe [17, 51, 64] and goat [81, 98, bSCC performed in various European 112, 114]. Thus, percentages of spontane- areas (European programme FAIR CT 95- ous cure during the dry period are generally 0881: ‘Strategies of in farm control of SCC lower in goats. If the infection substitutions in ewe’s and goat’s milk’). during the dry period are taken into account, these percentages are lower. The persistence of subclinical IMI dur- ing lactation is variable according to the causative pathogen but is generally high, 3.2. Effects of stage and number since Staphylococci represent the more fre- of lactation on the IMI incidence quent ones [132]. Subclinical IMI are in and prevalence general poorly detected and not eliminated at least during lactation. In two monthly 3.2.1. Lactation stage surveys concerning a total of 768 udder- halves during entire lactations (eight The incidence of clinical IMI does not months) in six dairy flocks, 45 to 50% of vary with the lactation stage in the same infected halves exhibited a single IMI way as in dairy cattle. A high incidence at
  • 6. 694 D. Bergonier et al. Table I. Geometric means of bulk milk somatic cell counts in various areas of the ewe’s and goat’s milk production (in thousands cells per mL) (Source: annual reports of the European programme FAIR CT 95-0881: ‘Strategies of in farm control of Somatic Cell Counts in ewe’s and goat’s milk’). Species Areas of production 1995 1996 1997 1998 1999 2000 Global (breed) Ewes Castilla-León (Churra) – – 783 866 916 – 863 Castilla-La Mancha 758 660 776 741 602 691 708 (Manchega) Spanish Basque country – 481 482 473 – – 477 (Latxa) Roquefort (Lacaune) 713 599 680 657 647 586 647 Pyrenees (Basco- 642 642 663 733 750 710 690 béarnaise, Manech) Sardinia (Sarda) 1561 1624 1566 1416 1457 1493 1509 Goats Castilla-La Mancha 2187 1259 1380 1318 1023 1071 1148 France (Alpine, Saanen) 1218 1111 1166 1226 1252 1309 1214 Sardinia (Sarda) 1595 1739 1516 1468 1483 1673 1575 drying-off or at parturition is observed in 3.2.2. Lactation number (parity) very rare and specific cases (mycotic agents or P. aeruginosa), in relation with An increased prevalence related to parity environmental contamination and/or poor has been reported in ewes and goats [26, 56, hygiene practices. On the contrary, the 80, 138]. Such descriptive data must be cau- higher rates are observed at the beginning tiously interpreted: the incidence is difficult of machine milking and during the first to differentiate from prevalence (chronicity third of lactation. High incidence may be or relapse), and older animals may be the observed in dairy ewes during suckling or more resistant ones. suckling-milking periods [22, 76, 80]. The variations of subclinical IMI inci- dence according to the stage of lactation 4. ANALYTICAL EPIZOOTIOLOGY should be assessed by systematic monthly milk culturing of large numbers of healthy udders. This kind of a study is very rare. 4.1. Sources and associated factors Variations can be indirectly estimated through SCC, allowing the analysis of large 4.1.1. Sources data sets. They must be cautiously inter- preted as infectious and milk dilution/con- The primary sources are firstly animal centration effects are added. In goats, carriage and subclinical IMI. The main sig- higher rates have been observed at the nificant Staphylococci reservoirs are sub- beginning of lactation [48, 128], but prev- clinical and chronical IMI and teat alence seems to increase throughout the cutaneous infections (traumas, contagious campaign (Fig. 3). In ewes, a high incidence ecthyma). CNS and S. aureus can also be was reported at the beginning of lactation cultured from healthy teat skin (and other [70, 80]. body sites or external orifices) ([27, 135],
  • 7. Mastitis of dairy small ruminants 695 Figure 3. Estimation of intramammary infection average prevalence throughout lactation in 155 French caprine herds [43]. Parturition took place in November and December. (Proportions of presumed infected udders were estimated through individual somatic cell counts.) Bergonier et al., unpublished results). Other vival of this organism [27, 153]. P. aerugi- bacteria also have animal primary sources: nosa, S. marcescens can survive in teat S. agalactiae, A. pyogenes, Mannheimia dipping solutions or disinfected moist clus- haemolytica, etc. The latter is carried in the ters (Bergonier et al., unpublished results). adults and suckling young’s mouth, naso- pharynx and tonsils [134]. 4.1.2. Factors associated to bacterial Other primary sources are environmen- persistence tal: Enterobacteria and Enterococci are found particularly in the litter, and Pseu- Udder infection persistence is due to the domonas spp. especially in water or a lack of precocious IMI detection and sys- humid environment. A. fumigatus and other tematic application of control programmes: fungi are isolated from mouldy forage, wet teat antisepsis, antibiotherapy or culling. bedding, litter, and air [110]. S. uberis and In French dairy ewe recorded flocks S. suis recognise mixed reservoirs: infected (379 flocks of the Roquefort area), foremilk animals, litter, and the environment. inspection is exceptional, udder palpation and California Mastitis Test (CMT) are The accessory sources are, for Staphy- occasionally realised by 57 and 65% of the lococci, housing, bedding, feedstuffs, farmers; post-milking teat antisepsis and air, insects, clusters, equipments, humans drying-off antibiotherapy are performed in (hands), other animals, etc. [3, 28, 139]. 20 and 70% of the flocks, respectively M. haemolytica can be found on the teat (Lagriffoul, 2000, unpublished results). skin of ewes soon after lambing [134] and These percentages are high compared to in the environment of diseased animals: other dairy ewe areas and are increasing. grass, water, straw bedding, etc. Colder, In French goat herds, drying-off antibio- wetter weather seems to prolong the sur- therapy frequency increased from 62.7%
  • 8. 696 D. Bergonier et al. in 1997 to 84.3% in 2000; teat antisepsis mine SCS across lactation [123, 124]. The progressed from 13.7 to 29.4% of the herds results are in close agreement with dairy [44]. cattle literature [125]. The genetic variabil- Extra-mammary bacterial persistence is ity of SCS in dairy ewes appears sufficient firstly due to hygienic or technical failures to implement a selection. The evolution of concerning the milking machine (over-used the genetic determinism of SCS during lac- liners, etc.). Very little literature is availa- tation shows a moderate to strong increase ble; incorrect machine disinfection (no in heritability. The values are particularly alternation acid-alkaline chlorinated water, low on the first test days (0.01 to 0.04), then too low water temperature) or the use of between the beginning to the middle of the rubber (vs. silicone) liners seems to be asso- lactation, estimates range from 0.04–0.1 to ciated with poorer tank milk bacterial 0.12–0.25 [9, 10, 83]. In dairy cattle, com- counts in ewes. parable studies reported a smaller increase with days in milk, with higher values in the Secondly, high stocking density, partic- first months of lactation [33, 36, 118]. ularly in intensively managed herds/flocks or during the suckling period, may result in Regarding relationships between udder large air concentrations of total microor- health and milk production traits, several ganisms, mesophilic or coliform bacteria studies indicate unfavourable positive and staphylococci. These effects are prob- genetic correlations between SCS and pro- ably associated with incorrect ventilation duction traits, ranging from 0.1 to 0.2 [9, 96, and high relative humidity. The multiplica- 124], as in dairy cattle [125]. Additionally, tion of various bacteria on the skin (and in the risk of being predicted as subclinically the litter) can be subsequently enhanced [2, infected (according to French SCC thresh- 137, 139]. olds) is significantly increased in the high, versus low, divergent lines selected on milk production in the La Fage experimental 4.2. Factors of susceptibility flock [9]. On the contrary, some authors found a favourable negative genetic corre- 4.2.1. Genetic factors: recent advances lation between SCS and milk yield, ranging from –0.35 to –0.11 [10, 49, 50, 83], con- Several studies on resistance to mastitis cluding that selection for increased milk have been recently based on SCC as an yield might not result in an unfavourable indirect way of measuring udder sanitary response for SCC. Discrepancies between status in dairy sheep (no literature data is the results could be due to differences in available in dairy goats). breeds, modelling and nature of the SCC data. Genetic parameters for SCC are calcu- lated after logarithmic transformation of 4.2.2. Environmental factors the values, i.e. somatic cell scores (SCS). The results based on repeatability test day Milking equipment and milking routine models for SCS indicate variable heritabil- are the main receptivity factors during lac- ity estimates from 0.04 to 0.17 [9, 10, 49, tation. In ewes, association between teat 63, 83]. Most studies based on larger data injuries and mastitis has been reported [5]. sets for the Churra and Lacaune breeds The limitation of udder massages and strip- reported consistent heritability values ping is associated with a significant positive between 0.11 and 0.15 for the lactation effect for primiparous goats: a decrease of mean SCS [9, 50, 123, 124]. A high genetic IMI and teat congestions. Over-milking correlation between the first and second limitation (respectively suppression) may lactation (0.88–0.93) has been reported, be associated with the reduction of hyper- indicating that mostly the same genes deter- keratoses (respectively reduction of minor
  • 9. Mastitis of dairy small ruminants 697 pathogen IMI prevalence), but data con- 5. DIAGNOSIS: cerning over-milking are rather inconsist- NEW DEVELOPMENTS ent; it is probably better tolerated by healthy IN THE CYTOLOGICAL udders [44]. A vacuum level increase may DETECTION OF MASTITIS induce a rise of SCC without clinical IMI [88, 140]. Clinical and bacteriological diagnosis Intramammary infusions at drying-off will not be considered, as recent advances or during lactation may cause teat duct cell mainly concern detection of subclinical damages. IMI by SCC. The factors affecting sensitivity are not very well known (very few data are availa- 5.1. Milk cell subpopulations ble about udder immunity). In dairy ewes, parenteral administration of vitamin E and Small ruminant milk contains the same selenium during the dry period can reduce types of cells as cow’s milk, but important SCC and increase the percentages of milk differences exist between ewe and goat neutrophils during the subsequent lactation milk cells in subpopulation percentages [102, 121]. Sensitivity may also be increased and total counts (Tab. II). by milk retention, due to a bad working In bacteriologically negative ewe’s milk, milking machine, under-milking, stressful epithelial cells seem to be less than 2–3% or painful milking and even udder morphol- of somatic cells, polymorphonuclear neu- ogy. Milk kinetics analysis allows to evi- trophil leukocytes (PMNL) constitute 10– dence too short milking times: 12 to 14% of 35%, macrophages 45–85% and lym- under-milking (1023 kinetics) have been phocytes 10–17%. These percentages do observed in goats [24]. not vary to a large extent with the lactation stage, excluding the beginning of lactation (particularly the colostral period) and the 4.3. Transmission involutive period: in early involution secre- tion, PMNL increase; they decline 21 days Spreading mainly occurs during milk- after cessation of lactation [78]. These per- ing. Udder massage and stripping induce centages are close to those of cow’s milk air intakes leading to impact. Cluster (2–30% for PMNL for example); in both removal by the milker may also induce species, the macrophage is the major cell type in bacteriologically negative milk [99, impact, since it is often performed without 106, 108]. There is a high correlation in previous vacuum cutting off (the automatic ewes and cows between PMNL percent- cluster removal is developing). Bacteria are ages and SCC [59, 103]. also transported passively by liners. How- ever, the IMI prevalences do not seem to be On the contrary, in goats, several cyto- significantly different between dairy (hand logical peculiarities must be underlined for or machine milked) and meat flocks. Trans- their biological as well as operational (IMI detection) interests. First of all, milk secre- mission is also possible by “milk-robber” tion in goats is apocrine [149, 150]: cyto- lambs (buccal carriage) and may be impor- plasmic particles are physiologically shed tant for staphylococci, Pasteurellaceae, into milk from the apical portion of secre- parapox virus (contagious ecthyma), etc. tory cells. Although most of them are anu- Penetration of the udder by organisms cleated, some of these particles have been is performed via the teat duct. In cases of observed to contain nuclear fragments systemic infections, haematogenous colo- [107] and could contribute to a slight extent nisation is frequent (lentivirosis, myco- to the total cell count. Cytoplasmic particles plasmosis, brucellosis, etc.). are similar in size to milk somatic cells.
  • 10. 698 D. Bergonier et al. Table II. Distribution of leucocyte subpopulations in small ruminant milk. Species Reference Year n Milk type Lactation (L.) Neutrophils Macrophages Lymphocytes stage % % % Goats [46] 1982 56 uninfected early L. 45 35 20 halves 4 uninfected late L. 74 15 9 halves [45] 1993 70 bulk tank 87.3 9.9 2.8 [122] 1993 200 halves weeks 1–4 pp 45.8 to 52.5 19.6 to 27.2 12.9 to 14.1 halves weeks 28–31 pp 68.6 to 70.3 12.0 to 12.5 2.9 to 4.3 [93] 1998 12 halves weeks 2–3 pp – 80 – weeks 4–18 50 45 – ³ 19 weeks pp 80 – – [52] 1999 950 halves – 40.9 35.6 0.7 [151] 2002 237 halves early L. 79 – 22 36 halves late L. 78 – 22 Ewes [55] 1985 84 uninfected mid-L. 26.5 to 58.5 – – halves 12 uninfected early drying-off 69.7 to 85.8 – – halves [59] 1985 91 halves mid-L. 10 to 90 0 to 60 8 to 18 [77] 1976 6 halves dry udder – 84 6 [78] 1981 6 halves colostrum 41 to 84 8 to 49 6 to 11 6 halves mid-L. – 83 to 86 10 to 17 [99] 1994 – uninfected whole L. 30 60 8 halves [100] 1996 640 uninfected whole L. 34.9 – – halves 50 infected halves whole L. 52.1 to 82.2 – – [101] 1996 10 healthy halves whole L. 30.6 57.3 8.2 [103] 2001 40 uninfected mid and 31.1 to 52.6 – – halves late L.* infected halves mid and 65.9 to 77.6 – – late L.* pp: postpartum. * No significant evolution according to the lactation stage.
  • 11. Mastitis of dairy small ruminants 699 Their average concentrations in milk is In goats, there is a little more informa- 150 ´ 103/mL for goats and 15 ´ 103/mL for tion concerning the relationship between ewes [108]. Furthermore, numerous inves- CAEV and SCC or the prevalence of sub- tigators reported unexpected SCC increases clinical IMI. A relationship between sero- and high PMNL percentages (Tab. II): logical status and bacterial IMI was PMNL comprise the major cell type in milk reported in herds with a high prevalence from uninfected goats [108]. In normal late of CAEV and IMI [62, 127, 129, 142]. lactation milk, they constitute 74–80% of This was attributed to a selective immuno- total cells. A significant increase has been suppression due to altered macrophage found in PMNL chemotactic activity dur- function during CAEV infection. In serop- ing this stage compared to early lactation ositive goats, an increase of SCC was and inverted evolution of mononuclear mostly reported as far as bacteriologically cells chemotactic activity. Differences uninfected halves are concerned [82, 105, between chemotactic cytokine profiles of 127, 130]. This could be related to the larger mastitic and normal late-lactation-stage number of macrophages in the milk of milk suggest the existence of a physiologic CAEV contaminated goats [82]. Neverthe- regulation in the influx of PMNL into the less, it was weak [82, 129] and lower than milk. The authors suspected PMNL to serve those due to bacterial infections. The effect as physiological regulators in the early of CAEV on SCC was not apparent when phase of the involution process [93]. In udder halves showed a persistent subclini- early lactation also, goat milk generally cal IMI. This failure of the inflammatory contains a higher PMNL proportion than response was interpreted as a reduction in the others. It has been suggested that leuko- the activity of macrophages caused by the cyte migration could proceed at a faster rate viral infection. Some cytokines, such as than that into cow’s milk and might contrib- chemotactic factors for neutrophils, and ute to naturally higher SCC [107]. The some mediators such as interleukin-8 could hypothesis of different defense mecha- be involved in this process [129]. nisms for the goat udder than for the bovine udder has been considered [97]. Some 5.3. Non-pathological variation factors authors suggest that in goats compared to of somatic cell counts dairy cattle, the low incidence of clinical IMI might be related to the physiologically The main variation factors for healthy high SCC and PMNL percentage. This udders are, in decreasing order of fre- hypothesis is weakened by the comparison quency, lactation stage, lactation number or with the ewes situation: the same low clin- within-day fluctuations, and milk fractions. ical IMI incidence and, on the contrary to The nature and importance of these factors goats, the same range of somatic cell counts have already been described [18, 60, 72, and percentages as in the cow. 108]. Briefly, in the ewe they are responsi- ble for geometric mean variations ranging 5.2. Lentiviral variation factors from 40 000 to 100 000 cells/mL, the mean of somatic cell counts iSCC values for uninfected ewe udders in mid-lactation ranging from 100 000 to The mammary gland of the goat and 250 000 cells/mL [18, 58, 108, 123]. The ewe is a target organ for lentiviral infec- lactation stage is the first of these factors. tions, but an additional difference between Irrespectively of the infectious status, SCC the two species is reported. In the ewe, no values increase as the stage of lactation clear evidence is available for influence of progresses, above all in goats (Figs. 4 and 5): Maedi-Visna infection on SCC at a large average values during the first three months scale [79]. are 200 ´ 103 cells/mL, and progressively
  • 12. 700 D. Bergonier et al. (b) Figure 4. The effect of lactation stage on individual somatic cell counts according to the infectious status of the mammary gland of ewes (a) (Rupp, unpublished results) and goats (b) [41, 94]. increase to more than 106 cells/mL during udders, whose SCC values show less the latter months [108]. In ewes, counts are fluctuations than those of goats, the ‘flock- higher during the first few weeks of lacta- campaign’ effect appears to be the most tion and decrease at the maximum milk important [123]. production. Average SCC (and PMNL per- Minor or punctual SCC variation fac- centages) are also affected by parity (Fig. 5) tors may exist according to the manage- [38, 41, 71, 122, 147]. For healthy ewe ment of the flock/herd. In ewes, the number
  • 13. Mastitis of dairy small ruminants 701 Figure 5. Illustration of the lactation number (parity) effect on individual somatic cell counts throughout the lactation of uninfected ewes [123] and goats [41]. Lac: lactation. of suckling lambs, the suckling-milking tion status among the indirect tests availa- period management, the lambing month, ble at the moment [14, 91]. and sudden dietary transitions are respon- sible for mild variations, whose geometric mean is generally lower than 20 000 cells/ 5.4. Recent advances in the practical mL [71, 72, 123]. In goats, vaccinations, use of individual somatic cell counts treatments, abrupt dietary modifications, stress, etc. have been found to increase SCC [82]. A significant SCC increase with 5.4.1. Punctual approach (and single a simultaneous decrease of production has threshold) been observed during induced estrus. This effect is accentuated in infected halves ([4, This simple and quite early methodol- 91], Poutrel, unpublished data). ogy proposes the punctual or instantaneous discrimination between ‘healthy’ and In conclusion, important differences ‘infected’ udders, generally using a single concerning differential and total counts, threshold. Thresholds are sometimes pro- lentiviral infection effect and non-patho- posed for milk to be tested bacteriologi- logical variation factors exist between cally. The threshold determination is dairy ewes and cows and, on the other usually based on the comparison of iSCC hand, goats. For the latter, cellular recruit- of punctually infected and uninfected ment is characterised by a more important halves, or on the choice of the best compro- number and diversity of factors, and by mise between sensitivity and specificity. greater inter-individual and temporal vari- Briefly, an analysis of the available litera- ations. The signification of goat milk cellu- ture bring forth the differences on the tech- larity fluctuations is not so far completely nical and methodological levels [40]. In understood. Nevertheless, bacterial IMI is goats, the apocrine character of lacteal the main variation factor of SCC, which secretion implies specific coloration of was found to be the best predictor of infec- DNA in order to differentiate cytoplasmic
  • 14. 702 D. Bergonier et al. particles from leukocytes [46, 152]. Large dynamic character of infection and cellular differences concerning the thresholds are response. Cut-off recommendations have also notable, even when considering stud- moved towards the use of consecutive iSCC ies using the fluoro-opto-electronic (FOE) per lactation and the definition of two (or method. The validity parameters (sensitiv- three) thresholds within the same detection ity, specificity, predictive values, etc.) of systems. An important reason is that sta- such detection methods are also highly var- phylococcal IMI are characterised by iable and consequently will not be reported. dynamic fluctuations and consequently cyclic milk shedding, potentially causing In ewes with the FOE method, the single false-negative bacteriological results. ‘Inter- thresholds proposed surprisingly range mittent isolations’ have been reported [27, from 200 000 to 1.5 million cells/mL; nev- 132]. This bacterial cyclicity is generally ertheless the majority of them are below inverted to PMNL one, since neutrophil 500 000 cells/mL [57, 58, 90, 95, 109, 119]. infiltrates usually eliminate most but not all Some authors suggested using two thresh- bacteria; SCC fluctuate according to the olds to distinguish ‘healthy’ from ‘infected’ organisms number and viability [39, 116, udders (140 000 and 340 000 cells/mL, 136, 148]. On the contrary, discordance [120]) or ‘minor’ from ‘major’ pathogen between some chronic IMI and SCC values IMI (244 000 and 106 cells/mL, [144]). is due to the important heterogeneity in CNS field strain virulence. For example in In goats, for healthy halves, arithmetic ewes, the SCC mean induced by S. lentus means with the FOE method range from is very close to that of uninfected halves 520 000 to 1.1 ´ 106 cells/mL [37, 41, 82, [14]. 113] and geometric means from 223 000 to 396 000 cells/mL [37, 41, 90]. The cut-off Consequently, one should prefer to use values range from 500 000 to 1.5 ´ detection systems defining a third class of 106 cells/mL [37, 67]. The studies and ‘doubtful’ udders and the combination of results differ depending on whether they several successive SCC, as in dairy cattle, consider the nature (‘minor’ versus ‘major’ rather than punctual approaches. A geo- metric mean is sometimes employed, but pathogens), intensity or persistence of IMI, generally one or several criterions based on and impact of non-infectious factors. the number of SCC exceeding the thresh- Among them, lactation stage has been pro- olds are used. Methodologically, these posed to be included in the definition of a proposed standards originate from the series of threshold values: according to cer- comparison of monthly SCC throughout tain authors, defining punctual standards the lactation to the results of monthly bac- for goat SCC is not possible without con- teriological analysis of udder-halve milk sidering lactation stage and probably parity samples. In goats, since 2000, development [60]. Using monthly SCC, a linear regres- of udder health management programmes sion allowed the determination of cut-off in France is based on a synthesis of two values from 556 000 cells/mL (90 days in studies [11, 41] (Tab. III) (SCC standards milk) to 1.2 ´ 106 cells/mL (305 days) [60]. are used for milk quality payment). The lat- ter defined thresholds related to various operational strategies, since the develop- 5.4.2. Dynamical approach and multiple ment of a single criterion is difficult in thresholds goats. Four criterions are proposed depend- ing on the nature of the infections, period of In addition to the necessity to take into detection (early lactation, drying off) and account these identified non-infectious var- practices (preventive or curative) for con- iation factors, other reasons explain that trolling IMI. In ewes (Tab. III), it is also studies have recently been focused on the possible to use geometric means or numbers
  • 15. Mastitis of dairy small ruminants 703 Table III. Dynamic approaches for somatic cell count detection of subclinical mastitis. Reference Year Infection type Criterion SCC N° Threshold Test validity parameters (%) Sens. Spe. PPV NPV Eff. Detection of infected goat halves [128] 1998 All infections Geometric 6 1 100 57.4 75.9 15.6 95.8 74.7 mean [65] 1990 All infections No. of over 800 62.5 87.0 61.4 92.5 80.9 counting: 2 Detection of infected goat udders [41] 1995 Minor pathogens No. of over 6 750 82.6 60.9 77.5 68.2 73.1 counting: 2 Major pathogens No. of over 6 1 750 61.3 80.2 16.5 97.0 79.2 counting: 3 [11] 1998 S. aureus No. of over C1 + 3 000 81.8 95.3 42.9 99.2 94.7 counting: 1 C2 S. aureus No. of over C3 to 2 000 73.3 91.2 33.3 98.3 90.2 counting: 3 Cn S. aureus No. of over C1 to 2 000 100.0 74.1 18.7 100.0 75.6 counting: 2 Cn All (primiparous) No. of over C1 to 600 90.9 85.7 90.9 85.7 88.9 counting: 2 Cn Detection of infected ewe udders [16] [14] 1996a Short infection or No. of over 2003 ‘doubtful’ counting: 3 Durable infection No. of over or ‘positive’ counting: 2 7 7 500 1 000 } 84.1 66.3 – – 71.1 Sens.: sensitivity; Spe.: specificity; PPV and NPV: positive and negative predictive values; Eff.: effi- ciency. Thresholds: ´ 1000 cells/mL. SCC: Somatic Cell Counts. SCC N°: number of SCC. of over counting, with thresholds and valid- 6. TREATMENT ity parameters close to those of the dairy cow [14, 16]. In both species, this kind of In small ruminant field conditions, clin- screening methodology can be adapted to ical and subclinical IMI treatments must be operational purposes (detection for culling, distinguished, the average treatment cost drying-off treatment, etc.) and sometimes per animal being high in comparison with to IMI prevalence assessment [90]. Usu- the culling value and the expected recov- ally, in field conditions, a few iSCC values ery. In (per)acute clinical cases, the first are available per lactation. In these cases, purpose is to save the animal’s life and, priority can be given to sensitivity, specif- possibly, to save the diseased halves. In icity, or predictive values in order to some areas, antibiotherapy is more and compensate for the decrease of overall effi- more used at drying-off, particularly for ciency. milk cellular quality control [22, 114].
  • 16. 704 D. Bergonier et al. Most of the published papers report ing bacteriological cure or prevention. The clinical observations and/or recommenda- overall cure rate ranges from 65 to 95.8% tions adapted from results obtained in the in the ewe [1, 35, 64, 86, 87] and from 50 cow; control-case studies are rare. Moreo- to 92.5% in the goat, whose dry period is ver, due to the general lack of specifically shorter [7, 54, 89, 112, 114]. The efficacy designed treatments for small ruminants, is better for CNS than for S. aureus infec- those for cattle are used (very few treat- tions. These cure rates are higher than ments are labelled for ewe and goat). spontaneous cure rates (see Sect. 3.1.2.). The preventive interest remains to be 6.1. Clinical mastitis discussed, particularly in ewes, considering No results from a controlled trial are the length of the dry period. Most bacteria available on the efficacy (i.e. bacteriologi- isolated from colostrum are not isolated cal and clinical cure) of parenteral or later in lactation (Berthelot, unpublished intramammary antibiotherapy. A clinical results). The new subclinical IMI rate at study about tilmicosin treatment of ovine lambing or kidding is therefore difficult to staphylococcal IMI and mammary derma- estimate (two successive bacteriological titis recently reported a complete symp- examinations are necessary). This rate is tomatology decrease five days after a single probably low, between 5 and 20%; very dose (10 mg/kg); this treatment seems to large data sets are therefore statistically also have induced a cessation of milk shed- needed to identify a possible positive pre- ding from days 5 to 7. S. aureus and CNS ventive effect of the drying-off treatment showed greater in vitro susceptibility to [1, 7, 17, 35, 87, 89]. tilmicosin than to various other antibiotics Different treatment strategies are per- [104]. Pharmacokinetics of various antibi- formed regarding the target for antibiother- otics have been studied after parenteral apy. Additionally to the dry period length in administration in the ewe and goat. Thera- ewes, three other small ruminant peculiar- peutical schemes have been proposed but ities should be taken into account: the large the efficacy has not been published so herd size, the production cycle synchroni- far: tobramycin (25 mg/kg) or apramycin sation inducing a collective drying-off, and (20 mg/kg) twice a day by intravenous from a pathological point of view, the low route; enrofloxacin (5 mg/kg) or norfloxacin drying-off and peri partum IMI incidences. (10 mg/kg) once a day by the intramuscular Consequently, a selective drying-off ther- route; tiamulin (25 mg/kg) twice a day by apy (concerning the infected udders only) the intramuscular route; florfenicol (20 to may be preferred to a systematic one. The 25 mg/kg) twice a day by the intravenous or limitation of the number of treatments intramuscular route [155]. Under field con- allows an easier implementation for a lower ditions, beta-lactamines and macrolides are cost and, overall, reduces the utilisation of still widely used via the intramuscular route, antibiotics and the risk of ‘iatrogenic’ udder as recommended in former studies [154]. contamination [22, 54]. Udder examination As in cattle, complementary treatments and iSCC or CMT are helpful to select the may be implemented in the severe cases ewes and goats requiring an antibiotic treat- [14, 47]. The economic interest of these ment. Drying-off antibiotherapy is gener- treatments and also of new antimicrobial ally performed once a year for the ‘whole’ drugs (fluoroquinolones) use remains to flock, but early dried females (including evaluated. subclinical IMI) mostly remain untreated [22]. For these females, antibiotherapy 6.2. Subclinical mastitis must not be implemented at this time by the The efficacy of drying-off intramam- intramammary route since the teat duct is mary antibiotherapy depends on consider- sealed by a keratin plug; the parenteral route
  • 17. Mastitis of dairy small ruminants 705 is the only usable one. An elegant possibil- During lactation, the infusion (three ity is to perform two (or three) successive syringes per udder-half at 12 h intervals) of sessions of intramammary infusion accord- a cattle-labelled formulation containing ing to the respective lactation durations. amoxicillin, clavulanic acid and pred- The intramuscular antibiotherapy (dry- nisolone led to the detection of residues up ing-off) would be an interesting route, par- to 136 h in the ewe and 112 h in the goat ticularly in large flocks, because it allows after the last infusion [30, 31]. In a similar an easier implementation and a reduction study, cloxacillin residues were detected in of the ‘iatrogenic’ risk of udder contamina- goat’s milk up to 156 h after the last infusion tion [155]. Nevertheless there is a lack of [61]. These results justify the 7-days with- published controlled trials. According to drawal period prescribed by the European field observations, two successive injec- regulation after an out-of-label intramam- tions at drying-off are needed to possibly mary treatment in lactating small rumi- obtain a significantly higher cure rate than nants. that of the untreated animals. After drying-off treatments of dairy ewes with a cattle-labelled formulation 6.3. Risks associated with containing penicillin (300 000 IU), nafcil- intramammary treatment lin (respectively 100 and 109.2 mg) and dihydrostreptomycin (respectively 100 and 6.3.1. Clinical outbreaks 125 mg), residues were detected at lambing in four (respectively five) ewes out of 190 The development of drying-off intramam- (respectively 25) and no more after three mary antibiotherapy has been associated (respectively 5) days [35, 84]. In goats in sheep and goats with a few outbreaks receiving the same formulation, residues of (per)acute to chronic clinical mastitis were found at kidding in some females caused by opportunistic pathogens, espe- whose dry period had been shorter than two cially P. aeruginosa (at the peri-partum months; no more residues were detected period and sometimes at the beginning of after seven days [85]. These results confirm dry period) or A. fumigatus (at the peri-par- previous data [54], who found residues tum period) [13, 66, 76, 110, 111, 117]. In in only 1 out of 34 treated goats after a most cases, the hygiene precautions had not 107-day dry period. been strictly respected at the time of imple- Considering the dry period durations, it mentation: teat-end disinfection, partial can be assumed that the risk of residues in and atraumatic introduction of the cannula, milk is virtually null at lambing and, a for- infusion of a complete syringe in each tiori, at the first milk delivery after a one to udder-half, teat antisepsis. Certain specific two-month nursing period. On the contrary, risk factors possibly existing at the time of in the goat, the risk at kidding is present, drying-off are now identified: liner contam- particularly in cases of a shortened dry ination originating from P. aeruginosa period (shorter than two months); in the lat- multiplication in machine residual water, ter conditions, a 14-day withdrawal period use of wet bedding or mouldy forage con- is justified, as recommended in the cow. taminated by A. fumigatus, etc. (Bergonier and Berthelot, unpublished results). 7. DISEASE CONTROL 6.3.2. Residues 7.1. Vaccination The risk of antibiotic residues in milk after intramammary treatments is poorly No literature relative to recent advances documented. in IMI vaccination is available since the
  • 18. 706 D. Bergonier et al. publication of a recent review [14]. Briefly, tions regarding the pen and the stocking regarding S. aureus, vaccine preparations density. based on bacterial cell extracts, capsular The control of environmental sources polysaccharides and/or toxoids, products of first consists in applying the pen recom- virulence regulation genes, adhesins, etc. mendations for its conception, maintenance have been proposed to prevent murine or and stocking density (primary sources). ruminant IMI. Attempts at immunisation The pen management plays a key role in with these preparations give generally controlling environmental bacteria IMI, insufficient results. In ewes, a liposome- and indirectly helps to reduce staphylococ- immunopotentiated exopolysaccharide vac- cal pressure through controlling density cine gave promising results [6]. Inactivated and air humidity. These factors are likely to vaccines and autovaccines are commer- enhance air and cutaneous staphylococcal cially available and widely used for ewes concentrations. Stocking density may rep- and goats in several countries. Information resent a critical factor in housing; too small about their efficacy in large scale controlled space allocations may adversely affect per- trials would be required. formances and health [137, 139]. For envi- ronmental pathogens, the greatest care 7.2. Preventive general management should be taken in the control of ambient hygiene, especially through efficient litter 7.2.1. Control of bacteriological sources management and ventilation systems [2]. This is of important concern in intensive production systems, particularly in goats. The control of animal sources first tar- gets intra-mammary carriage (primary Secondly, the liners must be replaced sources). This is mainly performed by dry- every year for rubber ones, every two years ing-off treatment of subclinical and mild for silicone ones. The milking machine chronic IMI and by culling the animals (liners, clusters, pipelines, etc.) must be who experienced acute or severe chronic cleaned disinfected twice a day with drink- IMI: udder asymmetry, diffuse hardness, ing water and following a validated proce- abscesses, etc. (abscesses must be differen- dure (accessory sources). tiated from cysts, generally located in declivitous position sagital and close to the 7.2.2. Control of bacteriological cisterns) [131]. After drying-off antibio- transmission during milking therapy, those animals still presenting chronic signs at the beginning of the subse- The milking technique represents a crit- quent lactation should be culled. ical point for IMI control, but the specific Mammary cutaneous carriage might be risk factors associated to each time of the controlled by pre-milking teat dipping; this milking routine – and the milking equip- measure is generally not used, due to herd ment – have not been completely character- sizes and milking routines, and probably to ised. Over- and under-milking and every the low incidence of bulk milk flora prob- factor leading to impact (brutal and pro- lems. In cases of staphylococcal dermatitis longed stripping, cluster removal without or contagious ecthyma, udder antisepsis, vacuum cutting off) must be avoided. isolation of affected animals and their Some authors underlined that preventive lambs, and sometimes antibiotherapy should practices, including milking techniques, be performed. The suckling lamb’s mouth were required to provide an effective and naso-pharynx carriage is important for decrease of IMI rates [44]. Minimising air staphylococci and M. haemolytica [3]. Its inlets contributed to significant improvement limitation relies on several other factors in udder health status as far as minor path- including the application of recommenda- ogens presumed infections were concerned.
  • 19. Mastitis of dairy small ruminants 707 Minimising mammary massage, machine 7.2.3. Limitation of receptivity stripping and avoiding the removal of extra- and sensitivity milk reattaching the teat cups is recom- mended, particularly for primiparous females. The non genetic control of udder recep- The effect of milking techniques on bSCC tivity is in particular based upon the reduc- were only significant at the end of the tion of teat lesions and pain caused by lactation (the middle or long-term effect). inadequate settings of the milking machine. A survey on standards for small rumi- Post-milking teat antisepsis seems to nants milking installations used in different allow a 30 to 40% decrease of new IMI in countries showed differences in ewes and the goat. The reduction is more important at goat husbandry leading to differences in the beginning of lactation, when spontane- requirements for milking equipment [24]. ous incidence is higher [12, 126]. The pos- Effective reserve, vacuum pump capacity itive effect on bSCC is also significant at and pulsation characteristics are especially the beginning of lactation [44]. Goat SCC in question. The lack of available knowl- analysis evidenced a decrease of primipa- edge prevents from taking into account rous early IMI and IMI recurrences [40]. In specific characteristics of species and another trial using iSCC but no bacteriol- breeds in construction and installations of ogy for the efficacy assessment, no differ- milking machines. Annual checking and ence was found between the dipped (nisin) regular maintenance of milking machines and undipped groups [114]. In dairy ewes constitute basic measures insufficiently also, teat-dipping or spraying is an efficient applied since only 40 to 60% of the total tool for reducing IMI incidence, above all number of machines are checked annually. in high prevalence situations (Berthelot Mostly, the purpose of the investigations et al., unpublished results). This preventive was to study the influence of machine measure is not frequently used, but could parameters on milking efficiency [53, 141]. be implemented for a limited duration, dur- Quantitative recommendations for small ing the period at risk (the suckling-milking ruminant milking installations were recently period or the beginning of milking after explored [25], with references to specific weaning) or for controlling a mastitis or equipments such as non conventional clus- teat dermatitis outbreak. Its precise effec- ters, references to specificity of milking tiveness according to the antiseptic mole- practices (attachment rates for example) cules and to the different prevalence and to typical lactation curves recorded in conditions remains to be evaluated in small various species and breeds. These recom- ruminants, mainly in the ewe. mendations will evolve during the next years and favour the development of relia- Implementing a milking order consists ble analysis of machine milking impact on in milking primiparous and/or healthy teat duct health. females first. In France, this heavy tech- The control of udder sensitivity should nique seems to be more frequent in goats be based on dietary recommendations: lim- than in ewes [44]. Its development may itation of sudden transitions or lack of bal- be associated with other advantages in ance. On the contrary, milk retention must goats regarding CAEV control, alimenta- be reduced through adaptation of the equip- tion or reproduction. Implementing a milk- ment to animal yield, teat size and flock ing order has been shown to be associated size [53]: vacuum pump capacity, vacuum with a decrease of (1) presumed major reserve, claws volume and position with pathogen associated IMI in primiparous regards to the liners. Automatic cluster goats, and (2) presumed minor pathogen removal systems, when they exist, must be associated IMI in multiparous goats [44]. carefully set.
  • 20. 708 D. Bergonier et al. 7.3. Genetic control The improvement of diagnosis would also need, especially in small ruminants, the The genetic basis of susceptibility to IMI development of rapid animal-side tests. The has been established (moderate heritabili- available tools are of limited interest: the ties and QTL for SCC). Effective inclusion foremilk visual examination and the Cali- of mastitis resistance in the breeding goal of fornia Mastitis Test can not be regularly and Lacaune breed, based upon SCC, has been systematically applied to large herds, and recently implemented in France [124]. the on-line electrical conductivity measure- Accordingly, breeders can choose their ment needs efficiency improvement and reproducer rams on mastitis resistance in technical adaptations to small ruminant addition to production traits (milk yield, fat milking machines. and protein contents) and PrP genotype The assessment of bacteriological cure (scrapie-resistant genotype). Improvement and new infection rates during the dry of resistance to mastitis by selection, how- period, with or without antibiotic treatment ever, is a long-term process and only par- at drying-off, require additional informa- tially efficient. Therefore, proper sanitary tion in order to define and accurately choose management remains the main clue to mas- the differential treatment strategies. Con- titis control. trolled trials are needed to better determine the bacteriological cure after drying-off intramammary or parenteral (two succes- 8. FUTURE PROSPECTS sive injections) antibiotherapy, according to the herd effects (main pathogens, infec- To control small ruminant mastitis, tions length). They will also provide infor- future research should concern the follow- mation about the new infection rates at ing fields, dealing with applied or basic lambing/kidding, in order to rationalise the research. choice between systematic and selective The improvement of diagnosis, particu- treatments and to assess the potential inter- larly IMI cytological detection in goats. est of teat sealers. Internal teat sealers are Future research in this field should attempt presumably less interesting in small rumi- to determine the exact impact on total and nants than in dairy cattle: the intramam- differential counts of CAEV, herd manage- mary implementation is not easier than ment factors (dietary or medical stresses, conventional treatments particularly for etc.) and physiological factors (lactation large flocks/herds, and the incidence of new stage, estrus, etc.). Non infectious varia- IMI during the dry period is lower. tion factors of SCC are unique in the case The assessment of preventive measures of goats in comparison with ewes and would be of particular interest regarding the cows; the inflammatory and immune proc- key-procedure in small ruminant IMI con- esses of the caprine udder are not com- trol: the milking machine management and pletely understood. This point must be the milking technique. Progress concerning underlined since SCC are the only large the former was published last year through scale available screening tests to be used quantitative recommendations for small for control programmes, and since maxi- ruminant milking machine installations mum levels are held as standards by the [25]. In the field, these recommendations dairy industry or health officials. Progress and the basic measures are insufficiently in this field could be achieved by charac- known and applied, and very different terising bacteriologically negative halves quantitative values are observed (particu- with high and low SCC, at different lacta- larly for pulsation rates). Moreover, addi- tion stages, from cytological, biochemical tional work is needed to clearly identify the and histopathological points of view. possible adverse effects of the equipment
  • 21. Mastitis of dairy small ruminants 709 and milking routines on the receptivity of [5] Ameh J.A., Tari I.S., Observations on the the mammary gland and on the spreading of prevalence of caprine mastitis in relation to predisposing factors in Maiduguri, Small organisms. Rumin. Res. 35 (1999) 1–5. The development of a new generation [6] Amorena B., Baselga R., Albizu I., Use of vaccine protecting against S. aureus IMI is liposome immunopotentiated exopolysac- an important need, this organism being the charide as a component of an ovine mastitis staphylococcal vaccine, Vaccine 12 (1994) main causative agent of acute and peracute 243–249. IMI. Immunity of the ovine and caprine [7] Anniss F.M., McDougall S., Efficacy of anti- mammary glands is still poorly under- biotic treatment at drying off in curing exist- stood. Possible means to achieve these ing infections and preventing new infections goals have been reviewed [116]. in dairy goats, in Proceedings of the 62nd Conference of the New-Zealand Society of The detection of the ovine genome Animal Production, Massey University, New regions involved in mastitis resistance Zealand, 24–26 June 2002, 62, pp. 19–21. began with the first results of a Quantitative [8] Ariznabarreta A., Gonzalo C., San Primitivo Trait Loci (QTL) detection program based F., Microbiological quality and somatic cell on purebred families of French dairy sheep count of ewe milk with special reference to breeds [133]. It showed that QTLs for SCS staphylococci, J. Dairy Sci. 85 (2002) 1370– 1375. were detected on chromosome 6 and 16, [9] Barillet F., Rupp R., Mignon-Grasteau S., allowing to locate the gene(s) that control Astruc J.M., Jacquin M., Genetic analysis for resistance to mastitis in this species. Addi- mastitis resistance and milk somatic cell tional and complementary results may arise score in French Lacaune dairy sheep, Genet. from another QTL programme, based on Sel. Evol. 33 (2001) 397–415. crossbreeding between Sarda and Lacaune [10] Baro J.A., Carriedo J.A., San Primitivo F., breeds, that was implemented in 1999 in a Genetic parameters of test day measures for somatic cell count, milk yield and protein Sardinian experimental flock [34]. Con- percentage of milking ewes, J. Dairy Sci. 77 versely to the previous project, the whole (1994) 2658–2662. genome will be investigated (genome [11] Baudry C., Mercier P., Mallereau M.-P., Lenfant scan), and traits related to mastitis resist- D., Utilisation des numérations cellulaires ance will also include information on clin- individuelles pour la detection des infections ical mastitis occurrence in addition to SCC. mammaires subcliniques de la chèvre : défi- nition de seuils, in Proceeding of the 6th Inter- national Symposium on the Milking of Small Ruminants, Athens, September 26–October 1, REFERENCES 1998 (1999) 119–123. [12] Baudry C., Mercier P., Mallereau M.P., [1] Ahmad G., Timms L.L., Morrical D.G., Lenfant D., Evaluation de l’efficacité du Brackelsberg P.O., Ovine subclinical mastitis post-trempage chez la chèvre, Rev. Med. Vet. efficacy of dry treatment, Sheep Res. J. 8 151 (2000) 1035–1040. (1992) 30–33. [13] Bergonier D., Berthelot X., Mammites asper- [2] Albenzio M., Taibi L., Muscio A., Sevi A., gillaires en élevage ovin laitier, Revue d’épi- Prevalence and etiology of subclinical masti- démiosurveillance VEGA 1 (1993) 10–11. tis in intensively managed flocks and related [14] Bergonier D., Berthelot X., New advances in changes in the yield and quality of ewe milk, Epizootiology and control of ewe mastitis, Small Rumin. Res. 43 (2002) 219–226. Livest. Prod Sci. 79 (2003) 1–16. [3] Albenzio M., Taibi L., Caroprese M., De Rosa [15] Bergonier D., Thiaucourt F., L’Agalactie G., Muscio A., Sevi A., Immune response, Contagieuse des petits ruminants, in: Lefèvre udder health and productive traits of machine P.C., Blancou J., Chermette R. (Coord.), milked and suckling ewes, Small Rumin. Res. Principales maladies infectieuses et parasi- 48 (2003) 189–200. taires du bétail. Europe et Régions chaudes, [4] Aleandri M., De Michelis R., Colafrancesco Ed. Tec et Doc, Lavoisier, 2003, 1824 p. R., Olivetti A., Valori citologici e agenti [16] Bergonier D., Van de Wiele A., Arranz J.M., infettivi di mastite nel latte de pecora, Atti Barillet F., Lagriffoul G., Concordet D., Berthelot Soc. Ital Sci. Vet. 38 (1994) 431–433. X., Détection des infections mammaires
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