Case-control studies of sporadic cryptosporidiosis in Melbourne and Adelaide, Australia
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Epidemiol. Infect. (2002), 128, 419–431. # 2002 Cambridge University Press
DOI : 10.1017\S0950268802006933 Printed in the United Kingdom
Case-control studies of sporadic cryptosporidiosis in
Melbourne and Adelaide, Australia
B. R O B E R T S O N ", M. I. S I N C L A I R "*, A. B. F O R B E S ", M. V E I T C H #, M. K I R K $,
D. C U N L I F F E %, J. W I L L I S " C. K. F A I R L E Y &
" Cooperatie Research Centre for Water Quality and Treatment at Department of Epidemiology and
Preentie Medicine, Monash Uniersity, Alfred Hospital, Prahran, Victoria 3181, Australia
# Microbiological Diagnostic Unit, Department of Microbiology and Immunology, Uniersity of Melbourne,
Australia
$ OzFoodNet, Australia New Zealand Food Authority
% Department of Human Serices, South Australia
& Department of Public Health, Uniersity of Melbourne, Australia
(Accepted 11 January 2002)
SUMMARY
Few studies have assessed risk factors for sporadic cryptosporidiosis in industrialized countries,
even though it may be numerically more common than outbreaks of disease. We carried out
case-control studies assessing risk factors for sporadic disease in Melbourne and Adelaide,
which have water supplies from different ends of the raw water spectrum. In addition to
examining drinking water, we assessed several other exposures. 201 cases and 795 controls were
recruited for Melbourne and 134 cases and 536 controls were recruited for Adelaide. Risk
factors were similar for the two cities, with swimming in public pools and contact with a
person with diarrhoea being most important. The consumption of plain tap water was not
found to be associated with disease. This study emphasizes the need for regular public health
messages to the public and swimming pool managers in an attempt to prevent sporadic
cryptosporidiosis, as well as outbreaks of disease.
of epidemiological studies suggest that the incidence
INTRODUCTION
of gastroenteritis in developed nations is around 0n7
Outbreaks of cryptosporidiosis have been studied episodes per person per year [2–6]. On this basis it can
extensively. The largest reported outbreak occurred in be estimated that in the United States during 1993
Milwaukee in 1993, when a drinking water supply waterborne gastroenteritis from recognized outbreaks
contaminated by Cryptosporidium was estimated to accounted for less than 0n25 % of all gastroenteritis,
have infected 403 000 people [1]. Because of drinking despite the occurrence of over 400 000 cases of illness
waters’ propensity to rapidly infect large numbers of from the Milwaukee Cryptosporidium outbreak [7]. It
people the primary focus of international and Austra- is important to establish risk factors for sporadic
lian research to date has been the cause of outbreaks cryptosporidiosis and examining the role of drinking
of cryptosporidiosis rather than factors contributing water as a risk factor for sporadic disease is considered
to sporadic disease. Sporadic disease however, may be particularly important.
numerically more common than outbreaks. A number We aimed to examine risk factors for sporadic
* Author for correspondence. cryptosporidiosis amongst the general communities of
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https://doi.org/10.1017/S0950268802006933420 B. Robertson and others
both Melbourne and Adelaide, Australia. These two years old, 40– 65 years old and 65 years old.
cities were chosen because they represent two extremes Telephone sampling using the Electronic White Pages
in raw water quality and treatment in Australia. (EWP) residential telephone directory was used to
Melbourne has high quality source water from highly recruit controls [10]. Prior to contacting a randomly
protected catchments which undergoes only minimal generated telephone number an introductory letter
treatment with chlorination [8], whilst Adelaide has was first sent to the household to improve par-
poor quality source water from unprotected catch- ticipation rates [11]. Approximately 2 weeks after the
ments which undergoes full conventional water treat- introductory letter, telephone calls to these numbers
ment including coagulation, sedimentation, filtration were then made, and a database of willing potential
and chlorination [9]. A case-control study design was controls was created in advance of cases over the
used to examine risk factors for sporadic crypto- course of the study.
sporidiosis. After a case was recruited and had the CATQ
administered, random potential controls of the same
sex and age bracket were automatically generated
from this database. If a suitably matched control was
METHODS
available the CATQ was administered, but if not then
Case-control studies were conducted in Melbourne a new randomly selected potential control was
from June 1998 to May 2001 and in Adelaide from generated until a control was eventually recruited.
November 1998 to May 2001. Ethical approval was Four matched controls were interviewed for each
obtained from the local institutional review commit- case. We attempted to administer the control question-
tees. Participants were recruited from the general naires within 3 working days of a case questionnaire.
communities of both cities. Controls were directly Only one control was recruited from each household
matched to cases according to age and sex, with four for each case, and the control was then retained in the
controls matched to each case. database of potential controls for possible selection at
We defined a case as having Cryptosporidium a later time. Controls were retained to prevent possible
oocysts detected in a faecal specimen by an accredited selection bias by their exclusion from the database
pathology laboratory, the onset of any diarrhoea or [12–14].
vomiting within 8 weeks before the administration of The CATQ inquired into demographic information,
questionnaire, residence in a household with a fixed clinical details of the case’s illness, education level,
telephone connection and the ability to speak English. employment, the consumption of tap water, the
Participating pathology laboratories sent reports of consumption of particular food groups, recreational
newly diagnosed cases of cryptosporidiosis to the water activities, the presence of immunological im-
Departments of Human Services in Victoria and pairment, the consumption of regular medication,
South Australia and these were forwarded to the contact with persons who may pose a risk of
Department of Epidemiology and Preventive Medi- cryptosporidiosis, animal contact, rural or overseas
cine (DEPM). With the permission of the case’s travel and exposure to child-care or breast feeding.
attending doctor, cases were recruited by telephone To isolate apparently sporadic cases, clusters of
calls. A maximum of nine telephone calls were made cases (and their matched controls) were removed from
to recruit individual cases. On contacting the case, or the database for analysis. The removal of clusters was
their main care-giver for children less than 12 years done by firstly identifying the symptom onset date of
old, the interviewer requested their consent to par- primary cases and then removing subsequent cases
ticipate. If consent was given, the computer assisted who had their symptom onset within a 14 day period
telephone questionnaire (CATQ) was administered if they either : resided within the same household,
immediately or at a mutually convenient time. attended the same swimming pool or attended the
We defined a control as not having diarrhoea or same childcare centre.
vomiting in the 2 weeks before the onset of the
matching case’s illness, residence in a household with
a fixed telephone connection and the ability to speak
Data analysis
English. Controls were matched to cases by sex and
the following age brackets : 1 year old, 1– 5 years The power of the study was calculated using drinking
old, 5– 12 years old, 12– 18 years old, 18– 40 water as the most important exposure to be assessed.
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https://doi.org/10.1017/S0950268802006933Sporadic cryptosporidiosis 421
For Melbourne with 201 cases and 795 controls the related exposures were examined from the same group
study had 80 % power, at 2-sided 5 % significance the most important single exposure based on pub-
level, to detect a trend in odds ratio (OR) of 1n22 per lished evidence was chosen.
quartile increase in the exposure [15]. For Adelaide
with 134 cases and 536 controls the study had 80 % RESULTS
power, at 2-sided 5 % significance level, to detect a
Melbourne
trend in OR of 1n28 per quartile increase in the
exposure. There were 271 cases reported in Melbourne during
Detectable OR (with 80 % power) for binary the study period. Of those, 201 (74n2 %) had the
exposures in the Melbourne study ranged from 1n6 for CATQ administered and were included in the analysis
an exposure with 50 % prevalence among controls to (Table 1). Twenty-four (8n9 %) had the CATQ
1n9 for 10 % prevalence. The corresponding detectable administered but were retrospectively excluded from
OR for Adelaide were 1n8 for 50 % prevalence to 2n2 the analysis because they were found to form disease
for 10 % prevalence. clusters, 14 (5n2 %) had the CATQ administered but
Data were analysed using Stata [16]. The standard were retrospectively excluded because it was admini-
analysis method for matched case-control studies is stered more than 8 weeks after their symptom onset,
conditional logistic regression when the matched sets 7 (2n6 %) cases refused to participate, 4 (1n5 %) doctors
are independent. However, in this study controls from refused permission, 11 (4n1 %) where case notification
the same household could be selected at multiple times to the DEPM failed, 3 (1n1 %) cases were unavailable,
for different cases, thereby inducing a correlation in 1 (0n4 %) did not have a fixed telephone connection, 1
the exposures across different matched sets, which (0n4 %) had an incorrect telephone number recorded
needed to be accounted for in the analysis. Standard and 5 (1n8 %) could not be contacted within 8 weeks of
conditional logistic regression was formulated as a symptom onset.
stratified Cox proportional hazard regression mode, Of the residential telephone numbers from which
with the matched sets as strata [17]. This allowed an the control sample was generated, letters were sent to
extension to accommodate the clustering effect of 5691 households. Of these, 3191 were contacted by
individuals from the same household using the telephone and were eligible to participate in the study,
‘ cluster ’ option in the ‘ stcox ’ command in Stata. In with 2177 (68n2 %) agreeing to participate. Of those
this way the Cox proportional hazards model was households agreeing to participate, 4322 individual
used to calculate crude and adjusted odds ratios for potential controls were recruited for the database,
the various exposures examined, together with 95 % with 795 CATQ administered to controls and included
confidence intervals (CI). Linear trend per unit being in the analysis, with 90 controls having conducted
measured (e.g. per glass of water consumed) or per more than one CATQ. For the 2500 households that
category being measured (e.g. per two glass categories were either not contactable or ineligible to participate,
of water consumed) was also calculated, together with 54 (0n9 %) letters were returned as the address was
95 % CI. Linear trend was used to evaluate a incomplete, 230 (4n0 %) had the maximum of 9
dose–response relationship when this was relevant. telephone calls exhausted without contact, 36 (1n0 %)
All exposures could not be adjusted for, because were ineligible because of a household member with a
many were highly correlated, making such an analysis chronic gastrointestinal illness, 302 (5n3 %) had insuffi-
numerically unstable. Because of the importance of cient English, 968 (17n0 %) had an incorrect phone
examining plain drinking water as a risk factor for number recorded, 126 (2n2 %) returned the letter as
sporadic cryptosporidiosis, this exposure was the there was a new resident, 773 (13n6 %) had not had all
main focus of the adjusted analysis. Individual 9 calls exhausted but calling was ceased because
confounding was sought by adjusting plain water sufficient numbers had been recruited and 11 (0n2 %)
against each exposure separately. Biologically plaus- were unavailable.
ible associations between exposures and plain drinking The median age for recruited cases was 11 years
water, and exposures and cryptosporidiosis were (range 0–81 years) and for controls 11 years (range
considered, particularly those that were statistically 0–83 years). One hundred and seven cases (53n2 %)
significant. Where possible there needed to be suffi- were male (Table 1).
cient numbers of participants in the exposed group to Cryptosporidiosis was not associated with the
achieve numerical stability. Finally, when a number of consumption of plain tap water. Neither the crude nor
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422
Table 1. Crude analysis with 95 % confidence interals (CI )
Melbourne Adelaide
B. Robertson and others
Crude OR*, Crude OR*,
Cases Controls 95 % CI Cases Controls 95 % CI
Number 201 795 134 536
Median age in years (range) 11 (0–81) 11 (0–83) 10 (0–83) 11 (0–86)
Male 107 (53n2 %) 428 (53n8 %) 67 (50 %) 268 (50 %)
Plain water
No 37 (18n4 %) 177 (22n3 %) 1n0 52 (38n8 %) 218 (40n7 %) 1n0
Yes 164 (81n6 %) 618 (77n7 %) 1n3 (0n9–1n9) 82 (61n2 %) 318 (59n3 %) 1n1 (0n7–1n6)
Plain water (glasses\day) (four categories)
None 37 (18n4 %) 177 (22n3 %) 1n0 52 (38n8 %) 218 (40n7 %) 1n0
0n01–2n00 64 (31n8 %) 225 (28n3 %) 1n4 (0n9–2n1) 32 (23n9 %) 117 (21n8 %) 1n2 (0n7–1n8)
2n01–4n00 42 (20n9 %) 216 (27n2 %) 0n9 (0n6–1n5) 29 (21n6 %) 98 (18n3 %) 1n2 (0n8–2n0)
4n00 58 (28n9 %) 177 (22n3 %) 1n6 (1n0–2n5) 21 (15n7 %) 103 (19n2 %) 0n9 (0n5–1n5)
Linear trend per one glass increase 1n05 (0n99–1n11) 0n98 (0n92–1n04)
P l 0n10 P l 0n47
Linear trend per one 1n11 (0n96–1n28) 0n98 (0n84–1n15)
category increase (four categories) P l 0n15 P l 0n85
Education level
0–12 years or schooling 33 (16n5 %) 125 (15n7 %) 1n0 27 (20n2 %) 118 (22n0 %) 1n0
Trade qualification 61 (30n5 %) 304 (38n2 %) 0n7 (0n5–1n2) 51 (38n1 %) 186 (34n7 %) 1n2 (0n7–2n0)
University 106 (53n0 %) 366 (46n0 %) 1n1 (0n7–1n7) 56 (41n8 %) 232 (43n3 %) 1n1 (0n7–1n7)
Work with sewage
No 94 (94n0 %) 360 (91n6 %) 1n0 59 (93n7 %) 237 (94n1 %) 1n0
Yes 6 (6n0 %) 33 (8n4 %) 0n7 (0n3–1n6) 4 (6n4 %) 15 (6n0 %) 1n1 (0n4–3n0)
Work in child-care
No 93 (93n0 %) 375 (95n4 %) 1n0 59 (93n7 %) 241 (95n6 %) 1n0
Yes 7 (7n0 %) 18 (4n6 %) 1n5 (0n7–3n5) 4 (6n4 %) 11 (4n4 %) 1n6 (0n6–4n3)
Work with animals
No 95 (95n0 %) 377 (95n9 %) 1n0 58 (92n1 %) 229 (90n9 %) 1n0
Yes 5 (5n0 %) 16 (4n1 %) 1n2 (0n5–2n9) 5 (8n0 %) 23 (9n1 %) 0n9 (0n4–2n1)
Uncooked carrots
No 88 (43n8 %) 270 (34n0 %) 1n0 55 (41n1 %) 166 (31n0 %) 1n0
Yes 113 (56n2 %) 525 (66n0 %) 0n6 (0n5–0n9)† 79 (59n0 %) 370 (69n0 %) 0n6 (0n4–0n9)†
Uncooked carrots
None 88 (43n8 %) 270 (34n0 %) 1n0 55 (41n0 %) 166 (31n0 %) 1n0
Monthly 26 (12n9 %) 110 (13n8 %) 0n7 (0n4–1n1) 18 (13n4 %) 88 (16n4 %) 0n6 (0n3–1n0)†
Weekly 55 (27n4 %) 279 (35n1 %) 0n6 (0n4–0n8)† 44 (32n9 %) 199 (37n1 %) 0n6 (0n4–1n0)†
Daily 32 (15n9 %) 136 (17n1 %) 0n7 (0n4–1n1) 17 (12n7 %) 83 (15n5 %) 0n6 (0n3–1n0)
Linear trend per one 0n85 (0n73–0n98)† 0n82 (0n70–0n99)†
category increase P l 0n02 P l 0n03https://doi.org/10.1017/S0950268802006933
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Unpasteurized milk products
No 194 (97n5 %) 784 (98n7 %) 1n0 130 (97n0 %) 531 (99 %) 1n0
Yes 5 (2n5 %) 10 (1n3 %) 2n0 (0n7–5n5) 4 (3n0 %) 4 (0n8 %) 3n9 (1n2–12n4)†
Swimming in public pool
No 103 (51n2 %) 550 (69n2 %) 1n0 97 (72n4 %) 411 (76n7 %) 1n0
Yes 98 (48n8 %) 245 (30n8 %) 2n5 (1n8–3n4)† 37 (27n6 %) 125 (23n3 %) 1n3 (0n9–2n0)
Swimming in public toddlers’ pool
No 163 (81n1 %) 710 (89n3 %) 1n0 122 (91n0 %) 509 (95n0 %) 1n0
Yes 38 (18n9 %) 85 (10n7 %) 2n3 (1n5–3n4)† 12 (9n0 %) 27 (5n0 %) 1n9 (1n0–3n6)†
Separate days in incubation period using public toddlers’ pool
No days 163 (81n1 %) 710 (89n3 %) 1n0 122 (91n0 %) 509 (95n0 %) 1n0
1 day 15 (7n5 %) 33 (4n2 %) 2n3 (1n3–4n1)† 2 (1n5 %) 10 (1n9 %) 0n9 (0n2–3n4)
1 day 23 (11n4 %) 52 (6n5 %) 2n2 (1n4–3n7)† 10 (7n5 %) 17 (3n2 %) 2n7 (1n3–5n4)†
Linear trend per 1 day increase 1n18 (1n08–1n30)† 1n24 (1n05–1n45)†
P l 0n0001 P l 0n019
Swimming in public adults’ pool
No 109 (54n2 %) 574 (72n2 %) 1n0 99 (73n9 %) 421 (78n5 %) 1n0
Yes 92 (45n8 %) 221 (27n8 %) 2n5 (1n8–3n4)† 35 (26n1 %) 115 (21n5 %) 1n3 (0n9–2n1)
Separate days in incubation period using public adults’ pool
No days 109 (54n2 %) 574 (72n2 %) 1n0 99 (73n9 %) 421 (78n5 %) 1n0
1 day 26 (12n9 %) 56 (7n0 %) 2n7 (1n7–4n3)† 7 (5n2 %) 27 (5n0 %) 1n1 (0n5–2n5)
2 days 25 (12n4 %) 101 (12n7 %) 1n4 (0n9–2n3) 13 (9n7 %) 49 (9n1 %) 1n2 (0n6–2n1)
2 days 41 (20n4 %) 64 (8n1 %) 3n7 (2n5–5n5)† 15 (11n2 %) 39 (7n3 %) 1n8 (0n9–3n3)
Linear trend per 1 day increase 1n18 (1n12–1n24)† 1n12 (1n04–1n22)†
P l 0n0001 P l 0n004
Immune system illness
No 193 (96n0 %) 792 (99n6 %) 1n0 126 (94n0 %) 530 (99n1 %) 1n0
Yes 8 (4n0 %) 3 (0n4 %) 14n0 (3n5–55n2)† 8 (6n0 %) 5 (0n9 %) 7n5 (2n7–20n8)†
Children at home in nappies
No 139 (69n2 %) 620 (78n0 %) 1n0 91 (68n4 %) 436 (81n3 %) 1n0
Sporadic cryptosporidiosis
Yes 62 (30n9 %) 175 (22n0 %) 1n6 (1n2–2n3)† 42 (31n6 %) 100 (18n7 %) 2n2 (1n4–3n2)†
Children 6 yr at home with diarrhoea
No 169 (84n5 %) 769 (97n2 %) 1n0 112 (84n9 %) 522 (97n8 %) 1n0
Yes 31 (15n5 %) 22 (2n8 %) 7n3 (4n2–12n5)† 20 (15n2 %) 12 (2n3 %) 7n1 (3n8–13n3)†
Children 6 yr at home attending childcare
No 152 (75n6 %) 691 (87n1 %) 1n0 105 (78n4 %) 476 (89n0 %) 1n0
Yes 49 (24n4 %) 102 (12n9 %) 2n2 (1n6–3n1)† 29 (21n6 %) 59 (11n0 %) 2n4 (1n5–3n8)†
Persons 5 yr at home with diarrhoea
No 169 (84n5 %) 726 (91n7 %) 1n0 103 (76n9 %) 491 (91n6 %) 1n0
Yes 31 (15n5 %) 66 (8n3 %) 2n1 (1n4–3n2)† 31 (23n1 %) 45 (8n4 %) 3n4 (2n2–5n3)†
Animal contact at home
No 101 (50n3 %) 311 (39n1 %) 1n0 54 (40n3 %) 162 (30n2 %) 1n0
423
Yes 100 (49n8 %) 484 (60n9 %) 0n6 (0n4–0n8)† 80 (59n7 %) 374 (69n8 %) 0n6 (0n4–0n9)†
[continued oerleaf ]https://doi.org/10.1017/S0950268802006933
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424
Table 1 (cont.)
Melbourne Adelaide
B. Robertson and others
Crude OR*, Crude OR*,
Cases Controls 95 % CI Cases Controls 95 % CI
Dog contact at home
No 128 (63n7 %) 445 (56n0 %) 1n0 75 (56n0 %) 259 (48n3 %) 1n0
Yes 73 (36n3 %) 350 (44n0 %) 0n7 (0n5–1n0)† 59 (44n0 %) 277 (51n7 %) 0n7 (0n5–1n1)
Cat contact at home
No 161 (80n1 %) 587 (73n8 %) 1n0 97 (72n4 %) 347 (64n7 %) 1n0
Yes 40 (19n9 %) 208 (26n2 %) 0n7 (0n5–1n0)† 37 (27n6 %) 189 (35n3 %) 0n7 (0n5–1n0)
Animal contact away from home, e.g. pet stores, farms, zoos
No 99 (49n3 %) 359 (45n2 %) 1n0 65 (48n5 %) 197 (36n8 %) 1n0
Yes 102 (50n8 %) 435 (54n8 %) 0n8 (0n6–1n1) 69 (51n5 %) 338 (63n2 %) 0n6 (0n4–0n9)†
Dog contact away from home
No 131 (65n2 %) 420 (52n8 %) 1n0 83 (61n9 %) 245 (45n7 %) 1n0
Yes 70 (34n8 %) 375 (47n2 %) 0n6 (0n4–0n8)† 51 (38n1 %) 291 (54n3 %) 0n5 (0n4–0n7)†
Cat contact away from home
No 160 (79n6 %) 622 (78n4 %) 1n0 117 (87n3 %) 398 (74n3 %) 1n0
Yes 41 (20n4 %) 171 (21n6 %) 0n9 (0n7–1n3) 17 (12n7 %) 138 (25n8 %) 0n4 (0n2–0n7)†
Calf contact away from home
No 184 (91n5 %) 770 (97n0 %) 1n0 129 (96n3 %) 528 (98n5 %) 1n0
Yes 17 (8n5 %) 24 (3n0 %) 3n1 (1n7–5n4)† 5 (3n7 %) 8 (1n5 %) 2n5 (1n0–6n4)
Lamb contact away from home
No 191 (95n0 %) 776 (97n7 %) 1n0 132 (98n5 %) 521 (97n2 %) 1n0
Yes 10 (5n0 %) 18 (2n3 %) 2n3 (1n2–4n6)† 2 (1n5 %) 15 (2n8 %) 0n5 (0n1–2n1)
Drink unboiled water from a country river, lake or dam within Australia
No 182 (90n6 %) 749 (94n3 %) 1n0 123 (91n8 %) 517 (96n5 %) 1n0
Yes 19 (9n5 %) 45 (5n7 %) 1n8 (1n1–3n0)† 11 (8n2 %) 19 (3n5 %) 2n4 (1n2–4n6)†
Travel overseas
No 174 (86n6 %) 781 (98n2 %) 1n0 127 (94n8 %) 531 (99n1 %) 1n0
Yes 27 (13n4 %) 14 (1n8 %) 8n6 (4n8–15n6)† 7 (5n2 %) 5 (0n9 %) 5n6 (2n1–14n6)†
Consume unboiled water, ice cubes or salad overseas
No 174 (86n6 %) 785 (98n7 %) 1n0 130 (97n0 %) 534 (99n6 %) 1n0
Yes 27 (13n4 %) 10 (1n3 %) 12n9 (6n4–26n1)† 4 (3n0 %) 2 (0n4 %) 8n0 (1n9–33n9)†
Participant breast fed if 3 years old
No 41 (91n1 %) 99 (86n1 %) 1n0 22 (100n0 %) 67 (89n3 %) 1n0
Yes 4 (8n9 %) 16 (13n9 %) 0n6 (0n2–2n1) 0 (0 %) 8 (10n7 %) –
Participant in child-care if 6 years old
No 35 (54n7 %) 127 (48n5 %) 1n0 18 (45n0 %) 82 (51n6 %) 1n0
Yes 29 (45n3 %) 135 (51n5 %) 0n7 (0n4–1n4) 22 (55n0 %) 77 (48n4 %) 1n4 (0n7–3n0)
* Adjusted for matching factors (age, sex) and family clustering.
† Bold type indicates statistically significant at P 0n05 level.Sporadic cryptosporidiosis 425
Table 2. Adjusted analysis with 95 % CI*
Melbourne Adelaide
Plain water
No 1n0 1n0
Yes 1n3 (0n9–2n1) 1n0 (0n7–1n6)
Pain water (glasses\day) (four categories)
None 1n0 1n0
0n01–2n00 1n4 (0n9–2n4) 1n1 (0n7–2n0)
2n01–4n00 1n0 (0n6–1n7) 1n2 (0n7–2n0)
4n00 1n5 (0n9–2n6) 0n8 (0n4–1n3)
Linear trend per one glass increase 1n04 (0n98–1n10) 0n96 (0n90–1n02)
P l 0n25 P l 0n21
Linear trend per one category increase (four categories) 1n10 (0n95–1n28) 0n95 (0n80–1n12
P l 0n21 P l 0n52
Educational level
0–12 years or schooling 1n0 1n0
Trade qualification 0n7 (0n4–1n3) 1n6 (0n9–2n9)
University 1n0 (0n6–1n6) 1n2 (0n7–2n1)
Uncooked carrots
No 1n0 1n0
Yes 0n6 (0n4–0n9)† 0n6 (0n4–0n9)†
Swimming in public pool
No 1n0 1n0
Yes 2n7 (1n9–3n8)† 1n2 (0n8–1n9)
Children 6 yr at home with diarrhoea
No 1n0 1n0
Yes 7n4 (4n0–13n8)† 8n6 (4n8–15n6)†
Persons 5 yr at home with diarrhoea
No 1n0 1n0
Yes 1n8 (1n1–2n9)† 3n7 (2n2–6n2)†
Animal contact at home
No 1n0 1n0
Yes 0n6 (0n4–0n8)† 0n6 (0n4–0n9)†
Calf contact away from home
No 1n0 1n0
Yes 2n9 (1n5–5n7)† 5n1 (1n5–17n3)†
Drink unboiled water from a country river, lake or dam within Australia
No 1n0 1n0
Yes 1n5 (0n8–2n7) 3n1 (1n5–6n5)†
* Adjusted for matching factors (age, sex), family clustering, plain drinking water (as dichotomous variable).
† Bold type indicates statistically significant at P 0n05 level.
adjusted OR for drinking any plain tap water dam within rural Australia, overseas travel and the
compared to no plain tap water was statistically consumption of unboiled water, ice-cubes or salad
significant. Similarly, there was no significant dose– overseas. Statistically significant protective factors
response relationship using a linear trend (Table 1). included the consumption of uncooked carrots,
For the crude analysis, statistically significant risk contact with any animal at home, dog contact at and
factors associated with sporadic cryptosporidiosis away from home, and cat contact at home.
included swimming in public pools (both toddler’s After performing an adjusted analysis on a limited
and adult’s), immune system impairment, having number of exposures (Table 2), swimming in public
children at home in nappies, having contact with pools, contact with persons with diarrhoea, and calf
children or adults with diarrhoea and having children contact away from home all remained statistically
at home attending childcare. Other risk factors significant risk factors, while the consumption of
included calf and lamb contact away from home, the unboiled rural water from a river, lake or dam within
consumption of unboiled water from a river, lake or Australia was no longer significant. Contact with any
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https://doi.org/10.1017/S0950268802006933426 B. Robertson and others
Table 3. Clinical features of cases
Clinical feature Melbourne Adelaide
Duration of illness (days)
Median (range) 21 (1–100) 15 (2–120)
Mean (range) 22n4 (1–100) 19n4 (2–120)
Hospital admission for one nights 14 (7n0 %) 16 (11n9 %)
Median number of nights (range) 2 (1–6) 2 (1–4)
Visits to the doctor
Median number of total visits (range) 2 (0–16) 2 (0–8)
Median number of visits before the visit at which the faecal 1 (1–5) 1 (1–6)
specimen was collected (range)
Symptoms
Diarrhoea present 198 (98n5 %) 132 (98n5 %)
Median stools per day when worst (range) 9n5 (1–40) 7 (1–40)
Mean stools per day when worst (range) 11n3 (1–40) 10n3 (1–40)
Watery motions 195 (98n5 %) 129 (96n3 %)
Bloody motions 17 (8n5 %) 8 (6n0 %)
Medication to stop diarrhoea 62 (31n3 %) 31 (23n5 %)
Vomiting 111 (55n2 %) 95 (70n9 %)
Abdominal pain 182 (90n5 %) 121 (91n7 %)
Felt hot 81 (40n3 %) 51 (38n1 %)
Time lost from study or work if participant 6 years old or more 101 (77n6 %) 59 (44n0 %)
Median number of days lost (range) 5 (1–21) 5 (1–77)
Time lost from study or work by family member other than case 76 (37n8 %) 52 (38n8 %)
Median number of days lost (range) 5 (1–28) 5 (1–77)
animal at home and the consumption of uncooked by another family member was a median of 5 days
carrots all remained statistically significant protective (range 1–28 days).
factors.
The clinical details of cases are described in Table 3.
The duration of the illness was a mean of 22n4 days
Adelaide
(range 1–100 days). Fourteen (7n0 %) cases required
hospital admission for 1 night or more, with a median There were 173 cases reported in Adelaide during the
stay of 2 nights (range 1–6 nights). Cases visited a study period. Of those, 134 (77n5 %) had the CATQ
doctor a median of 2 times (range 0–16 visits). The administered and were included in the analysis (Table
faecal specimen was usually collected on the first visit 1). Twenty-two (12n7 %) had the CATQ administered
to the doctor (median 1, range 1–5 visits). Diarrhoea but were retrospectively excluded from the analysis
was present in 198 cases (98n5 %). The number of because they were found to form disease clusters, 5
stools passed per day when the diarrhoea was at its (2n9 %) had the CATQ administered but were retro-
worst was a median of 9n5 and mean of 11n3 (range spectively excluded because it was administered
1–40 stools\day). One hundred and ninety-five (98n5 beyond 8 weeks of their symptom onset, 1 (0n6 %) case
%) reported watery motions and 17 (8n5 %) bloody refused to participate, 2 (1n2 %) doctors refused
motions. Sixty-two (31n3 %) reported the use of permission, 3 (1n7 %) cases were unavailable, 2 (1n2 %)
medication to stop their diarrhoea. For other symp- didn’t have a fixed telephone connection, 1 (0n6 %)
toms, 111 (55n2 %) reported vomiting, 182 (90n5 %) had an incorrect telephone number, 1 (0n6 %) could
reported abdominal pain and 81 (40n3 %) reported not be contacted within 8 weeks of symptom onset
feeling hot. Of those aged 6 years old or more, 101 and 2 (1n2 %) had insufficient English.
(77n6 %) lost time from study or work. The time lost Of the residential telephone numbers from which
from study or work was a median of 5 days (range the control sample was generated, letters were sent to
1–21 days). Of all cases, 76 (37n8 %) had another 4492 households. Of these, 2558 were contacted by
family member lose time from study or work so they telephone and eligible to participate in the study, with
could be cared for. The time lost from study or work 1766 (69n0 %) agreeing to participate. Of those
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https://doi.org/10.1017/S0950268802006933Sporadic cryptosporidiosis 427
households agreeing to participate, 3362 individual The clinical details of cases are described in Table 3.
potential controls were recruited for the database, The duration of the illness was a mean of 19n4 days
with 536 CATQ administered to controls and included (range 2–120 days). Sixteen (11n9 %) cases required
in the analysis, with 49 controls having conducted hospital admission for 1 night or more, with a median
more than one CATQ. For the 1934 households that stay of 2 nights (range 1–4 nights). Cases visited a
were either not contactable or ineligible to participate, doctor a median of 2 times (range 0–8 visits). The
49 (1n1 %) letters were returned as the address was faecal specimen was usually collected on the first visit
incomplete, 159 (3n5 %) had the maximum of 9 to the doctor (median 1, range 1–6 visits). Diarrhoea
telephone calls exhausted without contact, 23 (0n5 %) was present in 132 cases (98n5 %). The number of
were ineligible because of a household member with a stools passed per day when the diarrhoea was at its
chronic gastrointestinal illness, 192 (4n3 %) had insuffi- worst was a median of 7 and a mean of 10n3 (range
cient English, 696 (15n5 %) had an incorrect phone 1–40 stools\day). One hundred and twenty-nine (96n3
number recorded, 198 (4n4 %) returned the letter as %) reported watery motions and 8 (6n0 %) bloody
there was a new resident, 613 (13n6 %) had not had all motions. Thirty-one (23n5 %) reported the use of
9 calls exhausted but calling was ceased because medication to stop their diarrhoea. For other symp-
sufficient numbers had been recruited and 4 (0n1 %) toms, 95 (70n9 %) reported vomiting, 121 (91n7 %)
were unavailable. reported abdominal pain and 51 (38n1 %) reported
The median age of recruited cases was 10 years feeling hot. Of those aged 6 years old or more, 59
(range 0–83 years) and for controls 11 years (range (44n0 %) lost time from study or work. The time lost
0–86 years). Sixty-seven cases (50n0 %) were male from study or work was a median of 5 days (range
(Table 1). 1–77 days). Of all cases, 52 (38n8 %) had another
Cryptosporidiosis was not associated with the family member lose time from study or work so they
consumption of plain tap water. Neither the crude nor could be cared for. The time lost from study or work
adjusted odds ratio for drinking any plain tap water by another family member was a median of 5 days
compared to no plain tap water were statistically (range 1–77 days).
significant. Similarly, there was no significant dose–
response relationship using a linear trend (Table 1).
For the crude analysis, statistically significant risk
DISCUSSION
factors associated with sporadic cryptosporidiosis
included the consumption of unpasteurized milk This is one of the first case-control studies to examine
products, swimming in a public toddlers’ pool, risk factors for sporadic cryptosporidiosis in an
immune system impairment, having children at home industrialized country. Other studies have focused on
in nappies, having contact with persons with diarrhoea outbreaks of disease. Drinking water was not associ-
and having children at home attending childcare. ated with sporadic disease which is consistent with
Other risk factors included the consumption of findings from a randomized clinical trial recently
unboiled water from a river, lake or dam within rural conducted in Melbourne [6]. This study examined
Australia, overseas travel and the consumption of gastroenteritis rates in families receiving either plain
unboiled water, ice-cubes or salad overseas. Stat- or filtered tap water and found no evidence of
istically significant protective factors included the waterborne gastrointestinal disease. We found that
consumption of uncooked carrots, contact with any the risk factors for sporadic infection were generally
animal at or away from home, as well as dog and cat similar for both Melbourne and Adelaide despite
contact away from home. vastly different water supplies. These included risk
After performing an adjusted analysis on a limited factors commonly associated with outbreaks of
number of exposures (Table 2), contact with children disease, most importantly, swimming in public pools
and adults with diarrhoea, and the consumption of and person-to-person transmission. These results
unboiled rural water within Australia remained suggest that drinking water is unlikely to cause a
statistically significant risk factors, whilst calf contact significant amount of sporadic cryptosporidiosis in
away from home became statistically significant. major Australian cities.
Contact with any animal at home and the con- There were several specific exposures within the
sumption of uncooked carrots remained statistically swimming related group that were associated with
significant protective factors. sporadic cryptosporidiosis. The most consistent fea-
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https://doi.org/10.1017/S0950268802006933428 B. Robertson and others
ture for the two cities was an association with public Unpasteurized milk products such as cheese were
toddlers’ pools, which can be used by large numbers significantly associated with sporadic cryptosporidio-
of children. This source of recreational water activity sis for Adelaide but not for Melbourne. The small
was a biologically plausible risk factor for crypto- numbers in the exposed groups make it difficult to
sporidiosis, considering its faecal-oral transmission make deductions about differences between the two
route, the chlorine resistant nature of oocysts and the cities because of the limited statistical power. Unpas-
generally poorer hygiene habits of younger children teurized milk products are biologically plausible as a
which increase the risk of a faecal accident. In risk factor and have been associated with cryptospori-
addition, public pools have been associated with diosis previously [28, 29].
numerous previous outbreaks [18], including several The consumption of unboiled water from a rural
outbreaks in Australian cities [19–22]. river, lake or dam within Australia was a statistically
Person-to-person transmission was a risk factor for significant risk factor for Adelaide only. It is a
sporadic cryptosporidiosis in both Melbourne and biologically plausible risk factor since the microbio-
Adelaide. All types of exposures examined were logical quality of country water sources is highly
associated with disease. The strongest risk factor variable in Australia. These water sources are not
within this group of exposures was having young necessarily maintained in accord with drinking water
children at home with diarrhoea. This is not surprising quality guidelines, and may have livestock grazing
and is biologically plausible considering the route of along their banks, with such animals having been
transmission. Furthermore, it is well recognized as a implicated in the contamination of water sources
source of secondary transmission according to pre- overseas [30].
vious research [22–24]. Immune system illness, overseas travel and the
Calf and lamb contact away home were found to be consumption of unboiled water, ice-cubes and salad
statistically significant risk factors in Melbourne, overseas were strongly associated risk factors for
whilst only the former risk factor significant in sporadic cryptosporidiosis. Although biologically
Adelaide. Calves are reservoirs for Cryptosporidium plausible and having been associated with cryptospori-
oocysts and contact with these animals has been diosis previously, their OR are also likely to be
associated with cryptosporidiosis previously [25, 26]. inflated due to the ascertainment bias of cases. This
In contrast, various types of animal contact at home may be because overseas travellers who present to
were found to be protective factors. Other investi- their doctor with diarrhoea are more likely to have a
gators have suggested companion animals pose a faecal specimen requested, than those with diarrhoea
small risk [27]. A possible explanation for these who haven’t travelled overseas. Secondly, Melbourne
findings could be that animals kept at home shed and Adelaide pathology laboratories are more likely
oocysts to which occupants are regularly exposed, to test for Cryptosporidium oocysts in an overseas
which could confer active immunity. Adding to the traveller (unpublished data).
complexity is that some types of animal contact away We did not identify plain tap water as a risk factor
from home were also found to be protective, whereas for sporadic cryptosporidiosis in either Melbourne or
presumably this type of contact is more infrequent. Adelaide. The case-control studies allowed the op-
This area requires further attention to be more fully portunity to evaluate water supplies from different
understood. ends of the water quality spectrum. Melbourne has
Several food-related exposures were examined in- high quality source water from protected catchments
cluding some meats (sausage meat, hamburgers, offal), that undergoes very little treatment, whereas Ade-
lettuce and other leafy vegetables, uncooked berries, laide’s has poor quality source water that undergoes
uncooked mushrooms and uncooked carrots, but extensive treatment. Although drinking water has
none were identified as risk factors and uncooked been associated with many past outbreaks of crypto-
carrots were associated with a protective effect against sporidiosis, Melbourne’s drinking water supply was
sporadic cryptosporidiosis. The protective effect of not considered to be a likely source of disease prior to
regularly consumed raw vegetables has been identified this study because of its highly protected catchment
in unpublished outbreaks in the United Kingdom areas, with no public access or farming. In contrast,
according to Casemore [27]. The reasons behind the Adelaide’s drinking water supply was considered to
protective effect of only raw carrots remain specu- pose a greater risk of being associated with disease,
lative. because of its poor quality source water with few
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https://doi.org/10.1017/S0950268802006933Sporadic cryptosporidiosis 429
limitations on public access or farming. The results of estimates was possible for cases who suspected that a
this study however, suggest that the water treatment particular exposure was responsible for their illness.
processes currently in place in Adelaide are adequate Such a situation was only likely to occur on a large
to prevent waterborne sporadic cryptosporidiosis. scale if publicity was heightened at the time the study
The type of symptoms experienced by cases for was conducted, which linked cryptosporidiosis to the
Melbourne and Adelaide were typical of those exposure in question. In July to September 1998
reported by other investigators [31, 32], with the vast Sydney’s drinking water supply received substantial
majority of participants reporting watery diarrhoea local and international media attention when Crypto-
and abdominal pain. Symptoms were often severe and sporidium and Giardia oocysts were reportedly detec-
protracted, with a mean duration of 22n4 days (range ted, with three boil water advisories issued to the
1n0–100n0 days) and 19n4 days (range 2n0–120n0 days) public. This adverse publicity therefore adds further
for Melbourne and Adelaide respectively. The mean weight to the study finding that cryptosporidiosis is
number of stools passed per day when the diarrhoea not associated with the consumption of tap water. In
was at its worst was high ; 11n3 (range 1n0–40n0 stools) early 1998 prior to the commencement of the case-
and 10n3 stools (range 1n0–40n0 stools) for Melbourne control studies, several Melbourne swimming pools
and Adelaide respectively. were closed due outbreaks of cryptosporidiosis con-
The severity of disease reported by cases in this nected with the pools in question [19]. Considering
study was attributable to the selective effect of the most Melbourne cases were recruited at the end of
passive surveillance system by which cases were 2000 and the early part of 2001 it is unlikely that
recruited using laboratory notification. Such cases are biased reporting ensued. Furthermore, there were no
likely to represent only a small fraction of all swimming pool closures in Adelaide over the course of
cryptosporidiosis cases in the community as supported the study yet swimming in a public toddlers’ pool was
by overseas research [33], since only those with still found to be a statistically significant risk factor.
relatively severe symptoms are likely to seek medical The large numbers of exposures examined meant
attention and have a faecal specimen examined. In that some of the factors associated with crypto-
contrast, studies in volunteer subjects and outbreak sporidiosis might have been due to chance. To prevent
investigations with active case finding have reported ‘ data trawling ’ however, we only asked about ex-
less severe clinical symptoms and a shorter duration posures that were biologically plausible, or exposures
of disease. In the volunteer study by DuPont [31] the that had been previously associated with crypto-
mean duration of illness was 3n1 days (range 2n4–3n6 sporidiosis.
days), with a mean of 6n4 unformed stools per day A weakness of this study was that due to its
(range 4n0–11n0 stools) when the diarrhoea was at its relatively small size it did not have the statistical
worst. In the Milwaukee outbreak [1] people who had power to detect associations for uncommon exposures
clinical cryptosporidiosis which was not laboratory or exposures with small OR. For example, working
confirmed had a mean duration of illness of 4n5 days with sewage may be a significant risk factor but due to
(range 1n0–38n0 days), and a mean of 7n7 unformed only 6 % of Adelaide controls reporting this exposure
stools per day (range 1n0–60n0 stools) when the an OR of at least 1n9 would have needed to have been
diarrhoea was at its worst. For the 285 laboratory detected.
confirmed Milwaukee cases the disease was more In summary, this study suggests that drinking water
severe with a mean duration of 12n0 days (range is unlikely to be a major cause of sporadic crypto-
1n0–55n0 days), with a mean of 19n0 unformed stools sporidiosis in metropolitan cities of Australia. It
per day (range 1n0–90n0 stools) when the diarrhoea emphasizes three areas of public health importance.
was at its worst. Firstly, public swimming pools are an important
A methodological limitation of case-control studies potential source of large numbers of cryptosporidiosis
is recall bias of exposures, particularly when reliant on cases. This therefore reinforces the need for ap-
human memory [34]. Self-reported estimates for propriate and regular public health messages to the
exposures investigated such as drinking water intake public and swimming pool managers, in an attempt to
were likely to result in random rather than systematic prevent both sporadic disease and outbreaks. It also
error, which would have the effect of underestimating reinforces the need for close surveillance of swimming
the association between the exposure in question and pools by health departments to minimize outbreaks.
cryptosporidiosis. However, biased over-reporting of Secondly, education of the public about general
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https://doi.org/10.1017/S0950268802006933430 B. Robertson and others
hygiene measures to limit person-to-person trans- gastrointestinal health affects of drinking water quality.
mission needs to be undertaken. Thirdly, due to the Environ Hlth Perspect 2001 ; 109 : 773–8.
7. Kramer MH, Herwaldt BL, Craun GF, Calderon RL,
severity of illness in immunocompromised people, this
Juranek DD. Surveillance for waterborne-disease out-
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important risk factors identified from this study. 8. Melbourne Water Corporation – Website fhttp :\\
www.melbwater.com.au\g. 2001.
9. South Australian Water Corporation – Website
fhttp :\\www.sawater.com.au\g. 2001.
A C K N O W L E D G E M E N TS 10. Australia on Disc CDROM. Dependable Database
Data P\L, Sydney, NSW, Australia, 1998.
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JS. Selection of controls in case-control studies 1.
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Cooperative Research Centre for Water Quality and 13. Wacholder S, Silverman DT, McLaughlin J, Mandel
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