Yacoub A, Southgate BA. The epidemiology of schistosomiasis in the later stages of a control programme based on chemotherapy: the Basrah study. 1. Descriptive epidemiology and parasitological results. Trans R Soc Trop Med Hyg. 1987;81(3):449-59. doi: 10.1016/0035-9203(87)90165-9. PMID: 3120370.

1. TRANSACTIONS OF THE ROYAL SOCIETY OF TROPICAL MEDICINE AND HYGIENE (1987) 81, 449-459 449
The epidemiology of schistosomiasis in the later stages of a control
programme based on chemotherapy: the Basrah study. 1. Descriptive
epidemiology and parasitological results
ALIM YACOUB AND B. A. SOUTHGATE
Department of Tropical Hygiene, London School of Hygiene and Tropical Medicine, Keppel Street, London,
WCIE 7HT
Abstract
The association between infection with Schistosoma haematobium and various factors including
water contact pattern, past history of haematuria and treatment for schistosomiasisand cercarial
dermatitis was investigated in Southern Iraq. The study covered mainly primary schoolchildren in
different areasof Basrah and in Al-maadan locality where the majority of households with infected
schoolchildren occurred. Urine examination was by the sedimentation and Nuclepore liltration
methods. S. haematobium infection was very focal in distribution. There was evidence of local
transmission in the Al-maadan locality, while in Abu-al-Jawzi schistosomiasismight have been
acquired from endemic areasoutside Basrah governorate. Swimming, history of haematuria, and
history of treatment of schistosomiasis were significantly associatedwith the level of infection
determined by eggcount. Cercarial dermatitis, and bathing, washing clothes and fetching water were
not significantly associated. The prevalence of infection among male members of households of
infected children wassignificantly higher than that amongmalemembersof the remaining households
in Al-maadan. There was no evidence of clustering of casesat household level. The implications of
these findings for control and for future research on schistosomiasisin Basrah are discussed.
Introduction
What happens and what should be done in the late
stages of a schistosomiasis control programme?
Rational policy decisions on whether to increase
efforts to eradicate the infection or to maintain a low
cost “holding operation” can be made only by
carefully exploring the issues (BRADLEY, 1980).
Understanding of the dynamics of schistosomalinfec-
tion in a lowtransmission situation has so far been
annroached onlv on a theoretical basis. The analvsis
by MACDONALD (1965) led to the concept of ihe
break-point in the community worm burden, below
which the infection dies out. However, his analysis
was based on the assumption of random worm
distribution in the population; clumped (overdis-
persed)distribution, which is amore realistic assump-
tion based on field and autopsy studies, tends to
reduce the break-noint level (BRADLEY&MAY. 1978).
There exists an urgent need to obtain data‘on the
epidemiology of schistosomiasisin areaswhere a low
prevalencehasbeenattained following the application
of control measures.
Schistosoma haematobium infection is endemic in
Basrah,southern Iraq. A control programmebasedon
annual screening by urine examination of primary
schoolchildren (6 to 14 vears old) and selective
chemotherapy has been in *operation since the early
1960s.Hycanthone is the main drug used for treat-
ment. NAJAFUAN et al. (1961) reported a prevalence
rate of 86%among children 5 to 14yearsold north of
the city of Basrah, while no infection was reported in
Correspondence to be addressed to: Dr B. A. Southgate,
Department of Tropical Hygiene, London School of
Hygiene and Tropical Medicine, Keppel Street, London,
WClE 7HT
the southern zones.It wassuggestedthat the relative-
ly high salinity of water in the south due to tidal waves
from the Arabian Gulf provides an unsuitable habitat
for Bulks mmcatus snails, the intermediate host in
southern Iraq. Basedon recordskept by the Endemic
DiseaseCentre of Basrah. verv low nrevalence rates
among schoolchildren havebeenrepoited recently; in
1963the overall prevalence rate was 16%, while the
corresponding figures were 2.3%, 0*7%, 0.4% and
0.2% in 1965. 1969. 1975 and 1980 resnectivelv.
We report the results of an investigationcarried but
in depth to determine the prevalence and pattern of
distribution of S. huematobiuminfection in Basrah.
The investigation also aimed at identifying factors
which might have been responsible for the mainte-
nance of infection, albeit at low level, in this part of
Iraq. The association between the infection and
various factors including water contact pattern, past
history of haematuria, history of treatment for schis-
tosomiasisand arelated problem, cercarial dermatitis,
was investigated. We also attempted to examine the
distribution of infection at household level to find out
whether there was evidence of clustering.
Materials and Methods
snuly papulotion
Our approach was basedon screening by urine examina-
tion all orimarv schoolchildren in the studv areas. A
household
surveywascarriedoutin localitieswhereinfected
children lived. Such an approach has been proposed as a
system of monitoring transmission in areas where low
prevalence and intensity of infection have been achieved
(JORDAN,1977).
The field work was carried out during the period from
September 1983 to March 1984. (1) Initially, a detailed
searchwascarried out of the recordsof the Endemic Disease
Centre of Basrah where the results of school surveys were
reported for the period from 1970to 1983. Schistosomiasis

2. 450 EPIDEMIOLOGY OF SCHISTOSOMIASIS IN BASFUH. 1
MAYSAN
SCALE
Al-Hammar
Lake
N
BASRAH CENTRE
ARABIAN GULF
Arrows indicating the location of areas covered
by the epidemiological study:
@ Awesian 81 Bahadria
@ Al-ma jidiyah
@ Al-audiyah
@I Umm Al Naaj
Fig. 1. Map showing the location of different areas and districts within Basrah in relation to Shattal Arab River. (Urn Al Naaj referred to in paper
3 of this series.)

3. A. YACOUB AND B. A. SOUTHGATE 451
were detected by screening 1985schoolchildren in Awesian
and Bahadria; all came from known endemic areas in
Maysan and Dhiqar governorates, and spent each summer
with their relatives there, almost certainly acquiring their
infections during these summer visits. The problem of
infection acquired in distant endemic areasthus representsa
special problem in the epidemiology of declining schistoso-
miasis in Basrah, and is discussed in more detail by YACOUB
0985).
hasbeenmainly detected in recent yearsin Al-majidiyah and
Al-audiyah villages which are closeto eachother and about
30 km north of the city of Basrah (seeFig. 1). In the hrst
village prevalenceratesof 8%, 7% and 4% had beenreported
among male primary schoolchildren in 1978, 1979and 1980
respectively. The corresponding figures for females were
7%, 6% and 1%. Infection was reported for the first time in
Al-audiyah village in 1983;sporadic caseswere alsoreported
from Awesian and Bahadrta south of the city, anon-endemic
area in 1961. It was therefore decided to include Al-
majidiyah, Al-audiyah, Awesian and Bahadria in the school
survey (see Fig. 2).
(2) A list of all primary schoolsin theseareaswasobtained
from the Directorate of Education: all schools (one in
Al-audiyah, 2 in Al-majidiyah and 3 in Awes&n and
Bahadria) were coveredby the urine survey. An attempt was
made to examine all the schoolchildren. Each child was
asked to produce a specimen of urine in a glass tube.
Soecimens were allowed to sediment for one hour and
&iments were transferred to slides and examined in the
schools for ova of S. haemawbium. Those found infected
were asked to produce another specimen of urine to be
examined bv Nucleoore filtration as described below.
(3) Follo&ng th; Al-majidiyah and Al-audiyah school
surveys the households of children found infected were
located in Al-maadan locality, situated along the Al-
majidiyah river, a tributary of the main Shatt-al-Arab river.
This locality was covered by the household survey, the
results of which are presented in this paper. Only 5 cases
Fig. 2a
Diagram showing the
relative location of Al-
majidiyah and Al-audiyah
villages with respect
to Al-majidiyah River
The area is considered
the only focus for
bilharriasis in Basrah
(lam= soom)
-
a.xk
0
(4)‘An attempt was made to cover all the population in
Al-maadan locality by the household survey. Al-maadan
designates a group of tribes who originally lived in the
marshesand migrated in the early 1950sto settle in different
areasof Basrahincluding that along the southern side of the
Al-majidiyah river. There, they form a small community
convenient for the study of parasitological, serological and
behavioural asnects of schistosomiasis.The results of the
seroepidemiological survey are reported by YACOUB et al.
(1987).House-to-housevisits were carried out between 1100
and 1400h. Each member of the household was asked to
produce a specimen of urine in a plastic cup, and was then
interviewed according to a preceded questionnaire form
prepared to record information on age,sex, previous history
of haematuria, history of treatment for schistosomiasisand
history of swimmer’s itch (locally called shora).Information
was also obtained on various water contact activities at the
Al-majidiyah river, the main site of water contact for the
Al-maadan people, including swimming, bathing, washing
clothes and domestic utensils and fetching water. Other
BASRAH CITY
Fig. 2b
A diagram showing
the relative location of
Bahadria and Awesian villages
and schools covered by the
survey
Arrows indicate the schools
where cases of bilharziasis
were identified, and their
place of residence
Fig. 2. (a) Diagram showing the relative location of Al-majidiyah and Al-audiyah villages with respect to Al-majidiyah River.
(b) Diagram showing the relative location of Bahadria and Awesian villages and the schools covered by the survey.

4. 452 EPIDEMIOLOGY OF SCHISTOSOMIASIS IN BASRAH. 1
activities were either sporadic (like fishing, which predomi-
nantly involved the use of hooks) or were carried out in the
Shatt-al-Arab river which is free of B. rruncazus(such as
cutting grassand reeds).To minimize problems of recall, the
questions referred to water contact activities carried out in
the summer months prior to the survey (May to September
1983), the period of transmission in southern Iraq (EL-
GINDY, 1965; EL-GINDY & RADHAWY, 1965). Households
were categorized into 2 groups. Category 1 included
households of schoolchildren identified as parasitologically
positive by the initial school survey, while category 2
included the rest of the householdsin the samecommunity.
Suchclassificationwasthought to be useful in finding out to
what extent the level of infection can be reduced in a
community if a control programme, based on screening
schoolchildren and their familes and treating thoseinfected,
is to be implemented.
Laboratory procedures
The urine samplesobtained from infected schoolchildren
and from those covered by the household surveys were
examined by the Nuclepore filtration method described by
PETERS et al. (1976). 5 ml of urine were extracted by a
disposable syringe and injected through 12 urn pore sized
Nuclepore lilters loaded on 13mm filter holders; several
syringes-full of air were then assedthrough the filters. This
wasdonein the field and the iflter holders weretaken back to
Basrah Medical College Laboratory where they were dis-
assembled.The filters were placed facedown on glassslides
to be examined under a microscope using 40 x magnifica-
tion. In addition, 218 of 249 urine samplesobtained by the
household survey were examined by the sedimentation
method ascarried out for the schoolsurvey. The Nuclepore
and sedimentation methods gave identical results, 33 posi-
tive and 185negative samplesbeing found by each;however
the former was more rapid and accurate for the purpose of
quantification of schistosomeova.
Statistical anulyses
The analyseswere carried out in the following sequence.
(1) The individual associationbetween infection and eachof
the study variables was tested. The cm-square test with
continuity correction was used to assessthe significance of
the results. One way analysisof variance (F test) wasusedto
test the variation in the intensity of infection with age.
(2) Becausemany of the variables studied areinterrelated,
multiple regression analysis was applied to assess the
individual association’of eachvariable with infection, whilst
controlling for the other variables. Log,, (eggcount + 1)was
used asthe dependent variable while age, sex, water contact
activities, history of haematuria, history of treatment for
schistosomiasis,cercarial dermatitis and the category of the
householdwere the independent variables. The analysiswas
done using a computer program based on the statistical
packagefor the social sciences(SPSS);the stepwisemethod
wasused. Agewasrecordedasadummy variable to allow for
the non-linear relationship between age and infection.
(3) To confirm the results obtained from the multiple
regressionanalysis,logistic regressionanalysiswasapplied to
assess
the relative risk of infection associatedwith eachof the
dependent variables. The PECAN program, which usedthe
conditional maximum likelihood method of parameter
estimation for logistic regression models, was used for the
analysisof the resultsof the present study. Sincethe PECAN
program is mainly used for the analysis of case control
studies, our data were recodedto be fitted into the program.
Those positive for S. haematobium by urine examination
were considered as caseswhile those negative were consi-
dered as controls.
(4) Finally the results were tested for evidence of
clustering of infection at household level. A computer
program basedon a test described by SMITH & PIKE (1976)
was used to detect household aggregation of infection. The
test allows a generalization to be made to the situation in
which different population strata are at different risks of
infection. In our study, the test was used to allow for the
different age structures of individual households in the
Al-maadan locality. The information required to perform the
test wasthe number of individuals in different agegroups in
each household and the distribution of casesof schistoso-
miasis in these age groups.
School surveys
Results
The results of the school survey in Al-majidiyah
and Al-audiyah villages are shown in Table 1. 16
children were found to be infected with S. haemato-
bium, 11 in Al-majidiyah and 5 in Al-audiyah. All
casesdetectedin Al-majidiyah were maleswhile 3 out
Table I-Distribution and prevalence of S. haematobium infection by parasitology among primary schoolchildren in the
study area of Basrah
No. of households
No. of of infected
No. of children Type of school cases casesand their
Village in each school by sex (%) locations
Al-majidiyah 448 males ll(2.5) 10 Al-maadan*
Al-majidiyah 340 females -
Al-audiyah 206 mixed ~g:~ 5 Al-maadan
* Two of the infected schoolchildren from Al-maadan were brothers from the same household
Table 2-Distribution of S. huematobium infection by age and sex in Al-maadan locality
Age
(ye=)
<6
6-14
15-24
25+
TOTAL
Males
Number Number
examined positive
23 0
63 17
21 5
13 0
120 22
FC!ttl&S Total
Number Number Number Number
(“4 examined positive WI examined positive (“/a) X2 P
WJ) 15 1 (6.3) 38 1 (2-9
(27.0) 46 10 (21.7) 109 27 (24.8) 0;6 > 0.25
(23.8) 27 3 (11.1) 48 8 (16.7) 0.61 > 0.25
(0.0) 41 2 (4.9) 54 2 (3.7) - -
(18.3) 129 16 (12.4) 249 38 (15.3) 1.26 > 0.25

5. A. YACOUB AND B. A. SOUTHGATE 453
Table 3-Proportion of individuals who reported swimming by age and sex in Al-maadan locality
Males Females
Age Number % reported Number % reported
(years) interviewed swimming interviewed swimming
O-5 27 51.9 19 57.9
6-14 63 87.3 47 63.8
15-24 21 81.0 27 7.4
25+ 14 21.4 43 2.3
Total 125 71.2 136 32.3
x* = 30.78, P<0401 x2 = 52.33, F’<O401
Total proportions of males and females reporting swimming: x2 = 37.8, P<O,OOl
Combined
Number % reported
interviewed swimming
46 54.3
110 77.3
48 39.6
57 7.0
261 51.0
x2 = 77.2, df = 3, F<O.OOl
Table 4-Proportion who reported bathiig with respect to age and sex in Al-maadan locality
Age
(years)
6-14
15-24
25+
Total
Males Females
Number % reported Number % reported
interviewed bathing interviewed bathing
63 28.6 47 21.3
21 23.8 27 0.0
ii
14.3 43 0.0
25.5 117 8.5
x2 = 1.27, 0.50>&‘>0.25 (males only, all age groups)
x2 = 0.42, 0.9O>P>O.75 (males and females aged 6-14)
Table S-Proportions of females who reported washing clothes and fetching water with respect to age
Age
6-14
15-24
25+
Total
No. interviewed
47
G
117
% reported % reported
washing clothes fetching water
63.8 44.7
51.9 37.0
41.9 32.0
52.9 38.5
x2 = 4.37, x2 = 1.43,
0*25>P>O*lO 0.5O>P>O-25
of 5 casesin Al-audiyah werefemales.All the infected
children lived in Al-maadan locality. The geometric
mean egg output of the infected children was 8.3
eggs/5ml urine (95%confidenceinterval = 4-3-16.2).
General chat-act&sties of Al-maadan locality
45 households in Al-maadan locality were covered
by the survey. 261 individuals were interviewed, 125
males(48%) and 136females(52%); this wasthe total
permanent resident population of these households,
no attempt being madeto trace long-term adult male
absentees.About 60% of the population were below
15 years old. Adult men were either self-employed,
involved in various activities such as cutting grass,
fishing or, rarely, farming, or worked in skilled and
unskilled jobs for the government.
The distribution of infection by age and sex
Urine samples were obtained from 249 of 261
individuals. The prevalence rates of infection by age
and sexbasedon urine examination aregiven in Table
2. No significant difference wasdetectedbetween the
overall prevalence rates of males and females or
between the prevalenceratesof malesand femalesin
the 6-14 and 5-24 years age groups; tests of signi-
ficancewere not carried out for the O-5and 25+ years
old groups because of the less than 5 expected
frequencies in some cells.
The geometric mean egg output in those found
infected was9.4 eggsper 5 ml, 8.4 for malesand 10.2
for females (t = 0.28, P > O-5). The analysis of
intensity of infection amongthosefound infected with
respect to age was not significant (F = 2.46,
0.05 < P < O-1). The geometric mean egg output
among those found infected in the 6-14, 15-24 and
25+ year agegroups was 11*1,4*9 and 2.2 respective-
ly. The only female child below 6 years old who was
infected had an egg output of 290 per 5 ml.
Water contact pattern and its relation to schistosomiasis
Table 3 shows the proportion of individuals who
reported swimming during the summer prior to the
survey, by ageand sex. For all agegroups, except the
O-5 years old, males had higher water contact by
swimming than females.The maximum proportion of
those who swam during the summer prior to the
survey wasreported by the 6-14yearolds. The overall
difference betweenagegroups wassignificant for both
males and females.
The distribution of those who reported bathing
with respect to age and sex is shown in Table 4.
Children below 6 yearsold were mainly bathed in the
house and thus were excluded from the analysis.
Among males, there was no significant difference
between the remaining age groups with respect to

6. 454 EPIDEMIOLOGY OF SCHISTOSOMIASIS IN BASRAH. 1
Table 6-Infection with S. haematobium by mine examination and swimming, bathing, washing clothes and fetching water
Activity
SwiIIlkllg
Males Females Total
Number % Number % Number %
examined infected examined infected examined infected
22.7 25.0 132 31.5
i;
11:
::
5.9 117 -I;.;
120 129 12.4
x2 =
249
3.2, 0.05<P<O.10 x2 = 8.1, O~OOl<P<O~Ol
13.1
x2 = 13.4, P<O.OOl
25 28.0
No 20.8
Total ;: 22.7
-
Yes
No
Total
B+F (males only)
WyEhing
x2 = 0.21, 0*75>P>o~50
clothes(females)
No
Total
F;tsbing water (females)
No
62 16.1
1:: 1z
x2 = 055, 0.5O>P>O.25
45 13.3
69 13.0
Total 114 i3.2
x2 = 0.06, O+‘O>P>O*75
Table7-History ofhaemahuiaandtreatmentfor schistosomiasis history of haematuriaby ageis given in Table 7; about
by age 40% of children 6-14 years old gave such a history.
History of haematuria History of treatment
Age NlUUk Number
(Y=d interviewed % interviewed %
O-5 46 4.3 45 2.2
6-14 110 40.4 110 32.7
15-24 48 35.4 48 29.2
25+ 57 8.8 56 3.6
Total 261 26.1 259* 20.5
* 2 individuals could not answer this question
21 of 38 (55%) persons found infected by urine
examination reported a history of haematuria, com-
pared to 47 out of 211 who were negative by urine
examination. The difference was highly significant
(x2 = 16.0, P c O*OOl).
bathing. Bathing was reported by females6-14 years
old only; the proportion bathing wasnot significantly
different from males of the same age.
Washing clothes and fetching water were mainly
carried out by females above 5 years old. The
proportions of femaleswho reported these2 activities
are given in Table 5. There was no significant
difference between age groups.
The distribution by ageof thosewho gaveahistory
of treatment for schistosomiasisis alsogiven in Table
7. The pattern was similar to that of history of
haematuria, though the figures were consistently
lower. 34of 124(27.4%)malescomparedto 19of 135
females (14.1%) gave such a history, a significant
difference (x2 = 6.28, P < O*OOl). 13 of 38 found
infected (34.2%) gavea definite history of treatment,
comparedto 40 out of 215 (19%) who were negative
by urine examination; the difference was not signi-
ficant (x2 = 3.61, 0.10 > P > 0.05).
Cercariul detmatitis
Table 6 shows the distribution of infection with
respectto SW
imming (for malesand females),bathing
(for males) and washing clothes and fetching water
(for females).About 24% of individuals who reported
swimming were infected, compared with only 6%
among those who did not swim; the difference was
highly significant. The statistical difference wasmain-
tained for femalesbut it was just below the conven-
tional 5% significance level for males. There was no
significant difference with respect to infection status
between thosewho reported bathing, washing clothes
or fetching water and those who did not.
Information on cercarial dermatitis was gathered
from individuals aged6 years and older. About 45%
(96 of 215) reported this condition following contact
with water in the river. The onsetof the condition was
immediate following contact among 71% of cases,
while 29%reported the onsetwithin 1 h after going to
the river. Rash was associated with the itch in 91% of
cases:,in 45%it lastedfor lessthan oneday while 52%
said it lasted for one to 3 days. 21 of 37 individuals
infected with schistosomiasis(57%) reported cercarial
dermatitis, comparedto 75of 178(42%)who werenot
infected. Th; difference wa8 ndt significant
(x2 = 2.09, 0.25 > P >O*lO).
The an&sis by category of household
History of haematuti and treatment for schistosomiasis
68 of 261 persons gave a history of haematuria at
some time in the past. Among 125males, 45 (36%)
gavesuch ahistory comparedto 23out of 136females
(16*9%), a highly significant difference (x2 = 11.3,
P < 0.001). The distribution of individuals with a
The 15 households of the 16 schoolchildren found
infected in the initial school survey belonged to
category 1. 19 of 80 (23.3%) members of category 1
households (including the schoolchildren identified
by the survey) were infected, compared to 19of 169
(11.2%) infected in category 2. This difference was
statistically significant (x = 5*6,0*025 > P > 0.01).

7. A. YACOUB AND B. A. SOUTHGATE 455
The differences between the prevalence rates of
infection in the 2 categories for males and females
were mainly in males. 16 of 43 males (37%) in
category 1were infected, compared to 6 of 77 (7.8%)
males in category 2 (x2 = 14.0, P < 0.001). On the
other hand, females found infected in category 1
constituted 8.1% (3 of 37) compared to 14.1% (13 of
92) of females in category 2 (x2 = 1.52,
0.25 > P > 0.10).
In order to account for the differences in the
parasitological results between the 2 categories, we
examined the distribution of various demographic and
behavioural variables for the categories (Table 8).
There was no significant difference between the
categoriesof households with respect to age, sex or
any water contact activity (although swimming
approached the 5% significance level). The only
significant differences were related to history of
haematuria and treatment for schistosomiasis,where a
significantly higher proportion of individuals in categ-
ory 2 reported both theseconditions than did thosein
category 1. We also examined the distribution of
infection between the 2 categoriesallowing for ageby
the Mantel-Haenzel &i-squared test. There wasstill a
significantly higher prevalence rate of infection in the
first category (x2 = 4.42, 0.05 > P > O-025).
The results of the multiple and logistic regressionanalyses
The significant results of the multiple regression
analysis are shown in Table 9. Variables which were
entered in the final equation and which were signi-
ficantly associated with infection were swimming,
categoryof the household, history of haematuria, and
history of treatment for schistosomiasis.The tinding
that swimming was the sole water contact activity
associatedwith infection confirms the earlier analyses
(Tables 6 and 8). The negative sign attached to the
regression coefficient of the treatment variable indi-
catesthat this variable actedin the opposite direction
to the effect of others, i.e. those who had a history of
treatment for schistosomiasis were less likely to be
currentlv infected. These variables exnlained 17%of
the variance.
Results of the logistic regression analysis basedon
the PECAN programme are shown in Table 10 with
all the variables in the eauation. and in terms of the
relative risk of infection associatedwith eachvariable
controlling for the others. Significantly higher risk
was associatedwith swimming~ history of haematuria
and household cateeorv 1 (the lower limit of the 95%
confidence interval-was above 1). On the other hand
there was significantly lower risk associated with
history of treatment for schistosomiasis (the upper
limit of the 95%confidenceinterval wasbelow 1‘1.
It is
very interesting to observethat the variables shown to
be significant by both multiple and logistic regression
analysescanbe arrangedin the sameorder in termsof
their relative importance whether by using the
standardized regression coefficients or the relative
risks.
Results of the cluster analysis
Table 11 shows that there was no difference
between the expected and the observed number of
householdswith 0, 1,2 and more than 2 casesin each
household. The calculated expectednumber of house-
holds with zero caseswas 18.6 compared with the
observed 19; the results show no evidence of house-
hold aggregationof casesof S. haemutobium infection
in Al-maadan locality.
Discussion and Conclusions
The main enidemioloeical features of S. haemato-
bium infection-in Basrah are a low level of infection
and a focal pattern of distribution. Such features are
Table E-Distribution of age, sex, water contact activities, history
of haemataria, treatment for schistosomiasis and cercarial der-
matitis among members of the two categories of the households
Variable Category 1 category 2 Total
Age(YEW
O-5
6-14
15-24
25+
Total
x2 = 4.05, 0~5O>P>O~25
Sex
Males
Females
Total
x2 = 0.76, 0~50>2’>0.25
History of haematuria
Yes
NO
Total
x* = 7~14,0~005<P<0~01
History of treatment
Yes
No
Total
x2 = 10.91, P<O.OOl
Yes
No
Total
x2 = 3.72, O~OS<P<O.lO
Bathing*
Yes
No
Total
x2 = 0.022, 0.9O>P>O~75
Fetching water*
YeS
No
Total
x2 = 0.036, 0.9O>P>O.75
Washing clothes*
Yes
No
Total
x2 = 0.36, 0.75>P>O.S0
Cercarial dermatitis*
Yes
No
Total
x2 = 1.41, 0~25>P>O~lO
13 33 46
40 70 110
11 37 48
22 35 57
86 175 261
45 80 125
41 95 136
86 175 261
14 54 68
72 121 193
86 175 261
8 45 53
78 128 206
86 173 259
37 96 133
49 79 128
86 175 261
12 23 35
61 119 180
73 142 215
17 30 47
56 112 168
73 142 215
20 43 63
53 99 152
73 142 215
29 67 %
44 75 119
73 142 215
*Excluding children < 6 years old

8. 456 EPIDEMIOLOGY OF SCHISTOSOMIASIS IN BASRAH. 1
Table %Significant results of multiple regression analysis, using log,, (egg count + 1) as the dependent
varrable and age, sex, history of haematuria, treatment of schistosomiasis, cercarial dermatitis, category of
the household and water contact activities as the independent variables
Variable
Regression
coefficient (b)
History of 0.39
haematuria
History of -0.32
treatment
Swimming 0.18
Category of 0.15
the household
Constant -0.01
Multiple r = 0.4, rr = 0.17, standard error (r) = O-35
Standard
error (b)
0.09
0.11
o-05
o-05
0.04
P* t P
0.48 4.1 <O.OOl
-0.36 -2.9 <O.OOl
0.23 <O~OOl
0.19 ;:; <O*Ol
*Standardized regression coefficient
Table IO-Results of logistic regression analysis using PECAN computer programme (all variables in the
model)
Variable Relative risk (95% confidence interval)
Swimming*
Age (6-14)/25+ (females)
5.74 (1.54-21-32)
Age (6-14)/25+ (males)
0.95 (O-33-2.73)
Bathing
3.91 (0.67-22.74)
Washing
1.08 (0.41-2.87)
Fetching water
1.47 (0.35-6.16)
History of haematuria*
0.96 (0.26-3.78)
History of treatment for schistosomiasis*
13.02 (3.05-5-57)
Category of household (1) versus
0.18 (0.04-0.78)
category of household (2)*
444 (1.63-12.07)
History of cercarial dermatitis 0.50 (O-18-1.35)
*Significant at the 0.05 level
Table 11-Results of cluster analysis to detect aggregation of S. haematobium cases at the household level
No. of cases
per household
0
:
3+
Observed No.
of households
:;
;
Expected No. of
households
18.62
17.30
6.95
2.13
Total 45 45.00
Standardized normal deviate (SND, to test difference betweenexpectedand observednumber of householdswith
zero cases)= O-193; exact 2-tailed P = 0.847
x2 goodness of fit across all 4 categories= 0.73, df = 3, 09O>P>O*75
in completecontrast to thosedescribedin earlier work
in the samearea (WATSON,1950; NAJARIANet al.,
1961), when schistosomiasls was highly prevalent
throughout Basrah, including the city, except the
most southern part. The schistosomiasis control
programme launched by the Endemic DiseasesCon-
trol Centre, exclusively based on chemotherapy
among primary schoolchildren since 1965,must have
played an important role in changing the pattern and
level of infection, though the role played by other
factors such as improvements in standards of living
and ecological changesmust not be underestimated.
The high salinity and chemical pollution of the water
in the Shatt-al-Arab river might havemade conditions
unfavourable for the breeding of B. truncatus.
Another epidemiological feature of schistosomiasis
in Basrah, which can be considered as a recent
phenomenon, is the detection of infection in small
localities in known non-endemic areas which have
been recently settled by people from endemic areas

9. A. YACOUB AND B. A. SOUTHGATE 457
outside Basrahgovernorate. A more detailed study is
required to assess,in quantitative terms, the role of
human mobility in determining the spatial distribu-
tion of infection in this part of Iraq.
The datawhich have beenobtained from our study
cannot be used to support or refute the break-point
concept for the following reasons. (1) The original
observation of a persistently low prevalence rate
among schoolchildren in Basrah for the last 20 years
cannot be substantiated becausethe figures reported
were basedon pooling the results of surveys carried
out in villages which are completely heterogeneous
with respect to the pattern and levels of endemicity.
Even within a village (for example Al-majidiyah),
infection is usually confined to small localities (for
example Al-maadan). In addition, and becauseof the
mobility of the people to and from endemic areas,the
picture is further complicated by the detection of
casesin non-endemic areas.Furthermore, schistoso-
miasis has recently been detected among schoolchil-
dren in villages not covered by earlier surveys, or
where no records are available to ascertain whether
infection hasbeenintroduced recently or waspresent
before.
(2) The study identified an important factor which
might be responsible for the maintenanceof transmis-
sion in Al-maadan locality. Surveying members of
households of infected children identified by the
school survey led to the detection of only a few extra
cases(3 out of 19). The prevalence rate of schistoso-
miasis among members of this category was signi-
ficantly higher than that of other households in the
samelocality. However, this difference was confined
to males and was not significant between femalesin
the 2 categories. Thus, if the control programme is
basedmainly on school surveys, the current situation
in Basrah, there remains an important group in the
community, predominantly females,who could main-
tain transmission, though at low level.
(3) Becauseof the generally low observed preva-
lence and intensity of infection in the study areasof
Basrah, it is very likely that a proportion of positive
casesis missedduring any urine survey. The remain-
ing undiagnosedcases(assumingsuccessfulcure of all
the treated diagnosedcases)comprise the true preva-
lence for the next survey. This situation is unavoid-
able since, asthe prevalencedecreases,the predictive
value of parasitological tests(basedon urine examina-
tion in our study) is not expected to decrease
uniformly (GODDARD, 1977). The effect of multiple
urine examinations on consecutive days in such an
epidemiological situation is uncertain,- and deserves
further studv. WARREN
etal. (1978) showed that the
proportion of casescorrectly cl&&d according to S.
haematobiumegg count (including zero counts) was
75% based on a single urine examination; this
proportion rose to 78% when the classification was
basedon 2 specimens,and to 83%with 3 specimens.
KINGetal. (1982)in Qena, Egypt, showed that single
urine examinations underestimated prevalence rates
by about 20% and MANSOUR et al. (1981), working
near Cairo, increased prevalence rates by 10% by
examining 4 consecutive daily samples.
In addition to the category of the household, we
haveidentified 3 other factors which were significant-
ly associatedwith S. haematobiuminfection in Al-
maadan locality; these were history of haematuria,
treatment for schistosomiasis,and swimming. Other
factors including age, sex, cercarial dermatitis,
washing clothes, fetching water and bathing were not
significant as shown by the multiple and logistic
regression analyses.The finding that swimming was
the only water contact activity associatedwith acquir-
ing infection could be explained by the prolonged
water contact involved, the body surfaceareaexposed
and the multiplicity of sites frequented along the
Al-majidiyah river, which increase the chance of
encountering cercariae. Washing clothes, bathing,
and fetching water, on the other hand, were carried
out in selected sites and usually for short periods
when piped water was cut off, especially in the
daytime during summer. DALTON & POLE (1978),
employing a similar technique (i.e. multiple regres-
sion analysis), showedthat the pattern of S. haemato-
biuminfection in an endemiccommunity on the Volta
Lake in Ghana could be explained by exposure
through domestic and canoe-related activities, and
wasrelated to sex.However BARBOUR
(1985)analysed
the samedata, introducing ageasa variable factor to
allow for the non-linear relation between age and
infection, and showed that age and sex were the
signifkant factors which entered into the regression
equation. To allow for such a non-linear relation, in
our study agewas introduced as a dummy variable,
which serves the same function.
The negative association between history of treat-
ment and S. haematobiuminfection is worth noting.
Does this indicate that individuals acquire some
protection against reinfection following treatment?
Evidence of protection against reinfection with S.
munsoni following treatment with hycanthone of
Kenyan schoolchildren wasreported by STURROCK
et
al. (1983). BUTTERWORTH
et al. (1984, 1985) moni-
tored the rate of reinfection following treatment of
Kenyan children with S. mansoni under known
conditions of water contact; their study shows evi-
denceof age-dependentacquired resistanceto reinfec-
tion. Surprisingly, the variation in level of protection
was demonstrated within a very narrow age group.
Becauseour results were basedon retrospective data
and becauseinformation on time which had elapsed
since the individuals received treatment was not
available, we can only proposeahypothesis that some
cases of S. haematobium infection acquire some
protection following treatment; this needsto be tested
by further studies such as those of HAGANet al.
(1985a, b).
Cercarial dermatitis occurred irrespective of cur-
rent infection with S. haemutobium.This suggests
either that individuals in this area were frequently
sensitized by penetration of S. haematobiumcercariae
without further development of the parasites, or that
the condition wascausedby non-human schistosomes
(either S. bovis or Ornithobilharzia turkestanicum).
Certainly our findings do not suggestthe possibility
that sensitization to non-human schistosomesmight
confer a degreeof resistanceto human schistosomal
infection, as proposed by NELSONet al. (1962) and
termed “natural zooprophylaxis”.
There was no evidence of clustering of casesof S.
huemutobium
at household level in Al-maadan locality.
This might indicate that there was no variation
between individual households with respect to be-
havioural factors leading to infection. NOSENAS et al.

10. 458 EPIDEMIOLOGY OF SCHISTOSOMIASIS IN BASRAH. 1
(1975) could not find evidence of familial accumula-
tion of S. japmticum casesin an endemic community
in the Philippines by serological or parasitological
methods. However, evidenceof aggregationmight be
demonstratedif other criteria were used; for example,
we haveshown that there wassuchevidencewhen the
prevalence rates of infection were analysed with
respect to the 2 categoriesof households. Since the
only significant differences between these categories
were related to history of haematuria and history of
treatment for schistosomiasis (signilicantly more
among members of households of category 2 than
category l), asshown in Table 8, the lower prevalence
rate of infection in category 2 can be explained if the
hypothesis that successful treatment confers resist-
ance to reinfection is upheld.
In conclusion, the study demonstrates that the
distribution of S. huenuztobium infection in Bash is
highly focal in nature. Becausethe control program-
me using chemotherapy is basedmainly on screening
schoolchildren, the presence of undetected infected
individuals (predominantly females)in the commun-
ity might contribute significantly to the maintenance
of transmission, though at low level in Al-maadan
locality. Thus, in order to consolidate the effective-
ness of the control programme, screening of all
households in the identified localities needs to be
carried out. Swimming was identified as the main
water contact activity associatedwith acquiring infec-
tion. Further studies are required to explore the role
of non-human schistosomes in the causation of
cercarial dermatitis, to assess
the mobility of peopleto
and from endemic areasin determining the spatial
distribution of infection in Basrah, and to investigate
the rate of reinfection following treatment of children
infected with S. haematobium.
Acknowledgements
We would like to expressour gratitude to all the
schoolchildren and inhabitants of the Al-maadan localitv. for
without their cooperation this study would not havezbeen
feasible. Thanks go to the staff of the Endemic Diseases
Centre of Basrah for their help while carrying out the field
work. We would alsolike to thank Mr Richard Hayes of the
Tropical Epidemiology Unit, London Schoolof Hygiene and
Tropical Medicine, for his advice on the application of the
Smith & Pike test for cluster analysis. We thank Alison
Hinchley for typing the manuscript and for secretarial help.
Part of the material in this paper wasincluded in a thesis
by A. Yacoub acceptedfor the award of aPhD degreeby the
University of London.
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11. A. YACOUB AND B. A. SOUTHGATE 459
(1983).Observationson possibleimmunity to reinfection
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Accepted for publication 9 June 1986
Book Review
TIE Geography of Non-infectious Disease. M. R. S.
Hutt and D. P. Burkitt. Oxford University Press,
1986. 164 pp. (paperback f12.50)
Dennis Burkitt and Michael Hutt have spent much
of their professional lives studying variations in the
geographical pathology of disease,especially in Afri-
ca, and they have played an important role in
demonstrating the value of studying global, and more
restricted, variations in diseaseratesin the generation
of aetiological hypotheses. The literature on the
geographical distribution of diseasehas tended to be
concentrated in specialized journals though there has
been a crop of “cancer atlases” in recent years -
perhaps the most interesting being that for China,
showing remarkable variation in the ratesof common
cancers.Hutt and Burkitt have setout to give abroad
overview of the geographical distribution and causes
of non-infectious diseases,especially in non-western
countries. This they have done very well. It is an
ambitious undertaking not only becausethere arevery
many non-infectious diseasesbut alsobecausereliable
information on specific disease rates tends to be.
associated with the degree of development of the
country concerned, and the countries with the largest
diseaseburdens are generally those where systemsof
health statistics are poorest. Thus the information
that is pulled together is necessarily patchy in its
geographical coverage. The volume is sparing in its
use of maps and the authors gently suggestthat the
geographically illiterate might have a school atlas at
hand, Different chapterscover eachof the major body
systems:the alimentary tract; liver biliary systemand
pancreas;central nervous; cardiovascular; kidney and
urinary; respiratory; haemopoietic and lymphoreticu-
lar; male and female genital; breast; locomotor
system; and metabolism. For eachdiseaseconsidered
there aresectionson the geographicaldistribution and
postulated or possible causal factors. There is an
introductory chapter on environment and the causes
of disease and a short overview chapter which
discussesthe role of different factors asexplanations
for international variation in disease rates - not
unexpectedly, poverty and diet are identified as,
nrobablv, the major determinants for many diseases.
The specialist researcherin epidemiology or geog-
ranhical natholoav mav find the book a little frustrat-
ing becausethe%fo&ation on any one diseaseis
necessarilylimited, around 100diseases
being covered
in 140 pages.An impressive amount of information
hasbeenassembled?
however, from avery wide range
of sources and it is presented concisely and in an
attractive style. The authors make a convincing case
for the importance and interest of studies of geog-
raphical pathology in the developing world. In many
instancesdiseasesrateschangegreatly over compara-
tively short distancesand present tantilizing clues to
the environmental determinants of disease.
P. G. SMITH