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
6.1. Clinical mastitis .......................................................................................................................704
6.2. Subclinical mastitis ..................................................................................................................704
6.3. Risks associated with intramammary treatment ......................................................................705
6.3.1. Clinical outbreaks .........................................................................................................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
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 .
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 , 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 . 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 . 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% . 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 . The bSCC values and their corre-
. 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 . 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. . 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 . 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
Ewes Castilla-León (Churra) – – 783 866 916 – 863
Castilla-La Mancha 758 660 776 741 602 691 708
Spanish Basque country – 481 482 473 – – 477
Roquefort (Lacaune) 713 599 680 657 647 586 647
Pyrenees (Basco- 642 642 663 733 750 710 690
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 . 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 . 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 . 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  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
. cattle literature . 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 . 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 . 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 .
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 . 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 . 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 . 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-  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  1982 56 uninfected early L. 45 35 20
4 uninfected late L. 74 15 9
 1993 70 bulk tank 87.3 9.9 2.8
 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
 1998 12 halves weeks 2–3 pp – 80 –
weeks 4–18 50 45 –
³ 19 weeks pp 80 – –
 1999 950 halves – 40.9 35.6 0.7
 2002 237 halves early L. 79 – 22
36 halves late L. 78 – 22
Ewes  1985 84 uninfected mid-L. 26.5 to 58.5 – –
12 uninfected early drying-off 69.7 to 85.8 – –
 1985 91 halves mid-L. 10 to 90 0 to 60 8 to 18
 1976 6 halves dry udder – 84 6
 1981 6 halves colostrum 41 to 84 8 to 49 6 to 11
6 halves mid-L. – 83 to 86 10 to 17
 1994 – uninfected whole L. 30 60 8
 1996 640 uninfected whole L. 34.9 – –
50 infected halves whole L. 52.1 to 82.2 – –
 1996 10 healthy halves whole L. 30.6 57.3 8.2
 2001 40 uninfected mid and 31.1 to 52.6 – –
halves late L.*
infected halves mid and 65.9 to 77.6 – –
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 . 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 . 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 . 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 . 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 . The some mediators such as interleukin-8 could
hypothesis of different defense mecha- be involved in this process .
nisms for the goat udder than for the bovine
udder has been considered . 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 . are 200 ´ 103 cells/mL, and progressively
700 D. Bergonier et al.
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 . 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 .
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  and goats . 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 . 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 . 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
) or ‘minor’ from ‘major’ pathogen between some chronic IMI and SCC values
IMI (244 000 and 106 cells/mL, ). 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, .
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
. 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) . 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
 1998 All infections Geometric 6 1 100 57.4 75.9 15.6 95.8 74.7
 1990 All infections No. of over 800 62.5 87.0 61.4 92.5 80.9
Detection of infected goat udders
 1995 Minor pathogens No. of over 6 750 82.6 60.9 77.5 68.2 73.1
Major pathogens No. of over 6 1 750 61.3 80.2 16.5 97.0 79.2
 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
1996a Short infection or No. of over
2003 ‘doubtful’ counting: 3
Durable infection No. of over
or ‘positive’ counting: 2
} 84.1 66.3 – – 71.1
Sens.: sensitivity; Spe.: specificity; PPV and NPV: positive and negative predictive values; Eff.: effi-
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 . 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-
. 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 . 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 .
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
. 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 . Nevertheless there is a lack of . 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 . These results confirm
dry period) or A. fumigatus (at the peri-par- previous data , 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
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 . 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 . 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 .
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) . 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 . Minimising air
staphylococci and M. haemolytica . 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 .
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 . 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 . 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 . 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 , 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 . 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 : 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 . 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 . 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 . 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  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  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
 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 . 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  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 . It showed that QTLs for SCS staphylococci, J. Dairy Sci. 85 (2002) 1370–
were detected on chromosome 6 and 16,
 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  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 . Con- percentage of milking ewes, J. Dairy Sci. 77
versely to the previous project, the whole (1994) 2658–2662.
genome will be investigated (genome  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.
 Baudry C., Mercier P., Mallereau M.P.,
 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.  Bergonier D., Berthelot X., Mammites asper-
 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  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.
 Albenzio M., Taibi L., Caroprese M., De Rosa  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,
 Aleandri M., De Michelis R., Colafrancesco Ed. Tec et Doc, Lavoisier, 2003, 1824 p.
R., Olivetti A., Valori citologici e agenti  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
710 D. Bergonier et al.
subcliniques chez la brebis laitière à l’aide des  Billon P., Ronningen O., Sangiorgi F.,
comptages de cellules somatiques : proposi- Schuiling E., Quantitative requirements of
tions de seuils physiologiques, in: Rubino R. milking installations for small ruminants. A
(Ed.), Proceedings of Somatic cells and milk survey in different countries. Sixth Interna-
of Small Ruminants, International Sympo- tional Symposium on the Milking of Small
sium, Bella, Italy, Wageningen Pers, The Ruminants, Athens, Greece, in: Barillet F.,
Netherlands, 1996, pp. 41–47. Zervas N.P. (Eds.), Proceedings of the Sixth
International Symposium on the Milking of
 Bergonier D., Longo F., Lagriffoul G., Small Ruminants. Milking and milk produc-
Consalvi P.J., Van de Wiele A., Berthelot X., tion of dairy sheep and goats, Athens, Greece,
Fréquence et persistance des staphylocoques Wageningen Pers, The Netherlands, 1999,
coagulase négative au tarissement et relations pp. 209–215.
avec les numérations cellulaires chez la
brebis laitière, in: Rubino R. (Ed.), Proceed-  Billon P., Fernandez Martinez N., Ronningen
ings of Somatic cells and milk of Small O., Sangiorgi F., Schuiling E., Quantitative
Ruminants, International Symposium, Bella, Recommendations for Milking Machines
Italy, Wageningen Pers, The Netherlands, Installations for Small Ruminants, Bulletin of
1996, pp. 53–59. the International Dairy Federation 370 (2002)
 Bergonier D., Lagriffoul G., Berthelot X.,
 Boscos C., Stefanakis A., Alexopoulos C.,
Barillet F., Facteurs de variation non infec-
Samartzi F., Prevalence of subclinical masti-
tieux des comptages de cellules somatiques tis and influence of breed, parity, stage of lac-
chez les ovins et les caprins laitiers, in: tation and mammary bacteriological status on
Rubino R. (Ed.), Proceedings of Somatic Coulter Counter Counts and California Mas-
cells and milk of Small Ruminants, Interna- titis Test in the milk of Saanen and autoch-
tional Symposium, Bella, Italy, Wageningen thonous Greek goats, Small Rumin. Res. 21
Pers, Netherlands, 1996, pp. 113–135. (1996) 139–147.
 Bergonier D., Berthelot X., Poumarat F.,  Burriel A.R., Dynamics of intramammary
Contagious Agalactia of small ruminants: infection in the sheep caused by coagulase-
current knowledge about epidemiology, diag- negative staphylococci and its influence on
nosis and control, Rev. Sci. Tech. OIE, 16 udder tissue and milk composition, Vet. Rec.
(1997) 848–873. 140 (1997) 419–423.
 Bergonier D., Blanc M.C., Fleury B., Lagriffoul  Burriel A.R., Isolation of coagulase-negative
G., Barillet F., Berthelot X., Les mammites staphylococci from the milk and environment
des ovins et des caprins laitiers : étiologie, of sheep, J. Dairy Res. 65 (1998) 139–142.
épidémiologie, contrôle, in: Chabert Y. (Ed.),
Proceedings of Rencontres Recherches Rumi-  Burriel A.R., Dagnall G.J., Leukotoxic fac-
nants 4 (1997) 251–260. tors produced by staphylococci of ovine ori-
gin, Microbiol. Res. 152 (1997) 247–250.
 Bergonier D., Berthelot X., Romeo M.,
Contreras A., Coni V., De Santis E., Rolesu S.,  Buswel J.F., Barber D.M.L., Antibiotic per-
sistence and tolerance in the lactating sheep
Barillet F., Lagriffoul G., Marco J., Fréquence following a course of intramammary therapy,
des différents germes responsables de mam- Br. Vet. J. 145 (1989) 552–557.
mites cliniques et subcliniques chez les petits
ruminants laitiers, in: Barillet F., Zervas N.P.  Buswell J.F., Knigth C.H., Barber D.M.L.,
(Eds.), Proceedings of the Sixth International Antibiotic persistence and tolerance in the lac-
Symposium on the Milking of Small Rumi- tating goat following intramammary therapy,
nants. Milking and milk production of dairy Vet. Rec. 125 (1989) 301–303.
sheep and goats, Athens, Greece, Wageningen  Calavas D., Bugnard F., Ducrot C., Sulpice P.,
Pers, The Netherlands, 1999, pp. 130–136. Classification of the clinical types of udder
 Bergonier D., Lagriffoul G., Berthelot X., Le disease affecting nursing ewes, Small Rumin.
tarissement des brebis laitières : conduite et Res. 29 (1998) 21–31.
antibiothérapie. Journées nationales SNGTV-  Carnier P., Bettella R., Cassandro M., Gallo
INRA, Clermont-Ferrand, 30 mai–1er juin L., Mantovani R., Bittante G., Genetic param-
2001, pp. 295–299. eters for test-day somatic cell count in Italian
 Berriatua E., Ziluaga I., Miguel Virto C., Holstein Frisian cows, in: Proc. 48th Ann.
Uribarren P., Juste R., Laevens S., Vandamme Meet. Eur. Assoc. Anim. Prod, August 25–
P., Govan J.R.W., Outbreak of subclinical 28th, Vienna, Austria, 1997, p. 141.
mastitis in a flock of dairy sheep associated  Carta A., Barillet F., Allain D., Amigues Y.,
with Burkholderia cepacia complex infec- Bibé B., Bodin L., Casu S., Cribiu E.P., Elsen
tion, J. Clin. Microbiol. 39 (2001) 990–994. J.M., Fraghi A., Gruner L., Jacquiet P., Ligios
Mastitis of dairy small ruminants 711
S., Marie-Etancelin C., Mura L., Piredda G., comptages de cellules somatiques en élevage
Rupp R., Sanna S.R., Scala A., Schibler L., caprin, Proceedings of Rencontres Recher-
Casu S., QTL detection with genetic markers ches Ruminants 8 (2001) 157–160.
in a dairy sheep backcross sarda-Lacaune
resource population, N° 01-40 in 7th World  Droke E.A., Paape M.J., Di Carlo A.L., Prev-
Congress on Genetics Applied to Livestock alence of high somatic cell counts in bulk
Production, Montpellier, France, 2002. tank goat milk, J. Dairy Sci. 76 (1993) 1035–
 Chaffer M., Leitner G., Zamir S., Winkler
M., Glickman A., Ziv N., Saran A., Efficacy  Dulin A.M., Paape M.J., Wergin W.P., Dif-
of dry-off treatment in sheep, Small Rumin. ferenciation and enumeration of somatic cells
Res. 47 (2003) 11–16. in goat milk, J. Food. Prot. 45 (1982) 435–
 Charffeddine N., Alenda R., Carabano M.J.,
Genetic parameters for somatic cell score  East N.E., Birnie E.F., Disease of the udder,
within first lactation, and across lactations in in: Symposium on sheep and goat medicine,
Spannish Holstein-Frisian cattle, p32 in: Vet. Clin. North Am. (Large Anim. Pract.) 5
Proc. 48th Ann. Meet. Eur. Assoc. Anim. (1983) 591–600.
Prod., Vienna, Austria, 1997.  East N.E., Birnie E.F., Farver T.B., Risk fac-
 Contreras A., Sierra D., Corrales J.C., tors associated with mastitis in dairy goats,
Sanchez A., Marco J., Physiological thresh- Am. J. Vet. Res. 48 (1987) 776–779.
old of somatic cell count and California Mas-  El Saied U.M., Carriero J.A., San Primitivo
titis Test for diagnosis of caprine subclinical F., Heritability of test day somatic cell counts
mastitis, Small Rumin. Res. 21 (1996) 259– and its relationship with milk yield and pro-
264. tein percentage in dairy ewes, J. Dairy Sci. 81
 Contreras A., Paape M.J., Miller R.H., Prev- (1998) 2956–2961.
alence of subclinical intramammary infection  El Saied U.M., Carriero J.A., De La Fuente
caused by Staphylococcus epidermidis in a L.F., Genetic parameters of lactation cell
commercial dairy goat herd, Small Rumin. counts and milk and protein yield in dairy
Res. 31 (1999) 203–208.
ewes, J. Dairy Sci. 81 (1999) 2956–2961.
 Daley M.J., Oldham E.R., Williams T.J.,
 Esnal A., Romeo M., Extramiana B., Gonzalez
Coyle P.A., Quantitative and qualitative prop-
erties of host polymorphonuclear cells during L., Marco J.C., Mamitis en la oveja Latxa:
experimentally induced Staphylococus aureus eficacia del tratamiento y dinámica de infec-
mastitis in cows, Am. J. Vet. Res. 52 (1991) ción durante el período seco, in: XIX Jorna-
474–479. das Científicas Sociedad Española Ovino-
technica Caprinotechnica, Burgos, España,
 De Crémoux R., Poutrel B., Les numérations 1994, pp. 45–49.
cellulaires chez la chèvre : un outil de dia-
gnostic présomptif des infections mammai-  Fahr R.D., Schulz J., Finn G., Von Lengerken
res, Proceedings of the 7th International Con- G., Walther R., Cell count and differential
ference on goats, Tours, 15–21 mai 2000, cell count in goat milk – Variability and influ-
pp. 757–760. encing factors, Tierarztl. Prax. Ausg. G
Grosstiere Nutztiere 27 (1999) 99–106.
 De Crémoux R., Poutrel B., Berny F., Use of
milk somatic cell counts (SCC) for presump-  Fernandez N., Requena R., Beltran M.C.,
tive diagnosis of intramammary infections in Peris C., Rodriguez M., Molina P., Torres A.,
goats, in: Third Int. Mastitis Sem., Proceed- Comparison of different machine milking
ings II S6, 1995, pp. 90–91. clusters on dairy ewes with large size teats,
Ann. Zoot. 46 (1997) 207–218.
 De Crémoux R., Heuchel V., Berny F., Inter-
prétation des numérations cellulaires de lait  Fox L.K., Hancock D.D., Horner S.D., Selec-
de troupeau en élevage caprin : résultats pré- tive intramammary antibiotic therapy during
liminaires, Proceedings of the 7th Internatio- the nonlactating period in goats, Small
nal Conference on goats, Tours, 15–21 mai Rumin. Res. 9 (1992) 313–318.
2000, p. 764.  Fruganti G., Ranucci S., Tesei B., Valente C.,
 De Crémoux R., Heuchel V., Berny F., Valutazione dello stato sanitario della
Description et interprétation des comptages mamelle di pecore durante un intero ciclo di
de cellules somatiques des laits de troupeaux lattazione, Clinica Vet. 108 (1985) 286–296.
en élevage caprin, Proceedings of Rencontres  Fthenakis G.C., Prevalence and aetiology of
Recherches Ruminants 8 (2001) 163. subclinical mastitis in ewes of southern
 De Crémoux R., Heuchel V., Chatelin Y.M., Greece, Small Rumin. Res. 13 (1994) 293–
Évaluation des stratégies de contrôle des 300.
712 D. Bergonier et al.
 Fthenakis G.C., Use of somatic cell counts or isolated from subclinical mastitis in sheep,
of indirect tests in milk for the diagnosis of New Microbiol. 25 (2002) 367–373.
subclinical mastitis in ewes, in: Rubino R.
(Ed.), Proceedings of Somatic cells and milk  Kirk J.H., Glenn J.S., Mastitis in ewes, Comp.
of Small Ruminants, International Sympo- Cont. Educ. Pract. 18 (1996) 582–591.
sium, Bella, Italy, Wageningen Pers, The  Kirk J.H., Glenn J.S., Maas J.P., Mastitis in a
Netherlands, 1996, pp. 27–29. flock of milking sheep, Small Rumin. Res. 22
 Gonzalez Rodriguez M.C., Gonzalo C., San (1996) 187–191.
Primitivo F., Carmenes P., Rodriguez M.C.G.,  Lafi S.Q., Al Majali A.M., Rousan M.D.,
Relations between somatic cell count and Alawneh J.M., Epidemiological studies of
intramammary infection of the half udder in clinical and subclinical ovine mastitis in
dairy ewes, J. Dairy Sci. 78 (1995) 2753–2759. Awassi sheep in northern Jordan, Prev. Vet.
 Gonzalo C., Gaudioso Lacasa V.R., Evolu- Med. 33 (1998) 171–181.
tion des types cellulaires du laits de brebis  Lagriffoul G., Bergonier D., Berthelot X.,
(race Churra) en fonction des dénombre- Jacquin M., Guillouet P., Barillet F., Facteurs
ments cellulaires totaux pendant la traite de variation génétiques et non génétiques des
mécanique et manuelle, Ann. Zoot. 34 (1985) comptages de cellules somatiques du lait de
257–264. brebis en relation avec les caractères laitiers
 Haenlein G.F.W., Relationship of somatic et les mesures portant sur le lait de tank, in:
cell counts in goat milk to mastitis and pro- Rubino R. (Ed.), Proceedings of Somatic
ductivity, Small Rumin. Res. 45 (2002) 163– cells and milk of Small Ruminants, Interna-
178. tional Symposium, Bella, Italy, Wageningen
 Hill B.M., Jagusch K.T., Rajan L., Kidd G.T., Pers, The Netherlands, 1996, pp. 149–155.
Antibiotic residues in goats milk following  Lagriffoul G., Barillet F., Bergonier D.,
intramammary treatment, New Zeal. Vet. J. Berthelot X., Jacquin M., Relation entre les
32 (1984) 130–131. comptages de cellules somatiques du lait de
 Hinckley L.S., Revision of the somatic cell troupeau et la prévalence des mammites sub-
count standart for goat milk, Dairy Food cliniques des brebis estimée avec les compta-
Environ. Sanitat. 10 (1990) 548–549. ges de cellules somatiques individuels, in:
Barillet F., Zervas N.P. (Eds.), Proceedings
 Horstick A., Hamann H., Distl O., Estimation of the Sixth International Symposium on the
of genetic parameters for daily milk pre- Milking of Small Ruminants. Milking and
rformance of east Friesian milk sheep by ran- milk production of dairy sheep and goats,
dom regression models, in: 7th World Con- Athens, Greece, Wageningen Pers, The
gress on Genetics Applied to Livestock Netherlands, 1999, pp. 151–156.
Production, Montpellier, France, N° 01-53,
2002.  Lagriffoul G., Bergonier D., Bernard J.,
Millet F., Arranz J.M., Berthelot X., Barillet
 Hueston W.D., Boner G.J., Baertsche S.T., F., Situación de los recuentos de células
Intramammary antibiotic treatment at the end
somáticas en leche de oveja en Francia, Ovis
of lactation for prophylaxis and treatment of
intramammary infections in ewes, J. Am. 66 (2000) 29–34.
Vet. Med. Assoc. 194 (1989) 1041–1044.  Las Heras A., Dominguez L., Fernandez-
 Issartial J., La numération cellulaire indivi- Garayzabal J.F., Prevalence and etiology of
duelle du lait de chèvre : rôle du virus de subclinical mastitis in dairy ewes of the
l’arthrite encéphalite caprine (C.A.E.V.), Madrid region, Small Rumin. Res. 32 (1999)
Vet. Doct. thesis, Cl. Bernard-Lyon I Univer- 21–29.
sity, 1990.  Las Heras A., Dominguez L., Lopez I., Paya
 Jensen H.E., Espinosa de los Monteros A., M.J., Pena L., Mazzucchelli F., Garcia L.A.,
Carrasco L., Caprine mastitis due to aspergil- Fernandez Garayzabal J.F., Intramammary
losis and zygomycosis: a pathological and Aspergillus fumigatus infection in dairy ewes
immunohistochemical study, J. Comp. Pathol. associated with antibiotic dry therapy, Vet.
114 (1996) 183–191. Rec. 147 (2000) 578–580.
 Kalogridou-Vassiliadou D., Manolkidis K.,  Lee C.S., Outteridge P.M., The identification
Tsigoida A., Somatic cell counts in relation to and ultrastructure of macrophages from the
infection status of the goat udder, J. Dairy mammary gland of the ewe, Ajebak 54 (1976)
Res. 59 (1992) 21–28. 43–55.
 Kanellos T.S., Burriel A.R., Production and  Lee C.S., Outteridge P.M., Leucocytes of sheep
novel quantification of haemolysins pro- colostrum, milk and involution secretion,
duced by coagulase-negative staphylococci with particular reference to ultrastructure and