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The association between drinking water source

and colorectal cancer incidence in Jiashan
County of China: A prospective cohort study

Article in The European Journal of Public Health · January 2006

DOI: 10.1093/eurpub/cki027 · Source: PubMed

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 European Journal of Public Health, Vol. 15, No. 6, 652–656
Ó The Author 2005. Published by Oxford University Press on behalf of the European Public Health Association. All rights reserved.
doi:10.1093/eurpub/cki027 Advance Access published on July 28, 2005
............................................................................................................
Cancer
............................................................................................................
The association between drinking water
source and colorectal cancer incidence in
Jiashan County of China: a prospective
cohort study
Kun Chen1, Weiping Yu1, Xinyan Ma2, Kaiyan Yao1, Qinting Jiang3

Background: The pollution of drinking water, e.g. from rivers and pools, has long been recognized
to be associated with an increased risk for colorectal cancer (CRC), but there are few direct prospective
cohort studies related to person-years on the relative risks of different sources of drinking water for
CRC, hence the reason for our study. Methods: Based on a screening for CRC among residents aged
30 years and over in Jiashan County, Zhejiang Province, China, a total of 64,115 residents were classified
into five cohorts by their source of drinking water and followed-up from 1st May 1990 to 1st January 2001.
Person-years was calculated for every cohort member and Poisson regression was used to control poten-

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tial confounding variables including demographic variables and smoking history, and to attain crude
and adjusted relative risks based on person-years. Results: A trend was seen toward increasing incidence
rates for CRC from the drinking water sources of municipal, river, ditch, mixed water to well in turn as
shown by relative risk rates of 29.61, 32.67, 33.45, 40.87 and 58.67 per 100,000 inhabitants. Only the role
in risk of well water was significantly different from municipal water (P < 0.05). After the confounding
variables were adjusted, the significant risk from well water could be seen for colon cancer, rectal cancer
as well as CRC. The relative risks were 1.741 [95% confidence interval (CI) 1.001–3.029], 2.228 (95% CI
1.432–3.466) and 2.022 (95% CI 1.432–2.854), respectively. Conclusion: Drinking well water over a long
period was identified as playing a role in the risk for CRC, especially for rectal cancer.

Keywords: cohort study, colorectal cancer, drinking water source, Poisson regression
............................................................................................................

olorectal cancer (CRC), including rectal cancer and colon
C cancer, is one of the most common cancers. It has been
estimated that more than half a million people annually become
new CRC cases throughout the world. In the USA, CRC is the
fourth most common cancer (after lung, prostate and breast)
and the second most common cause of cancer death (after lung)
(1). Recently the incidence has increased, especially in the
developing world with the change towards more western
diets. China is a nation with a relatively low incidence of
CRC, but in the eastern part of China there has been a higher
incidence of CRC reported. Jiashan County has been shown to
have the highest incidence of CRC in China, with the mortality
rate of 26.3/100,000 per year in males and 18.6/100,000 per year
in females (2).
The pollution of drinking water has long been recognized to
be associated with an increased risk of cancer in some epidemi-
ological studies (3–5), including several studies concerning
chemical and microorganism contamination (6–8). We carried
out a prospective cohort study with person-years directly on
the relative risks of different sources of drinking water for
CRC in Jiashan County, Zhejiang Province, China.
.............................................................
1 Department of Epidemiology, Zhejiang University School of
Medicine, Hangzhou, People’s Republic of China
2 Cancer Institute of Jiashan-county, 314100 Jiashan Zhejiang,
People’s Republic of China
3 Department of Biology Chemistry, Hong Kong City University,
Hong Kong
Correspondence: Prof. Kun Chen, Department of Epidemiology,
Zhejiang University School of Medicine, 353 Yan’an road, Hangzhou
Zhejiang 310031, People’s Republic of China, tel: þ86 571 8721 7190,
fax: þ86 571 8721 7184, e-mail: ck@zjuem.zju.edu.cn
Materials and methods
Study cohort and baseline exposure
From 1st May 1989 to 30th April 1990, screening for CRC was
carried out among 75,842 residents aged 30 years and over in 10
small towns in Jiashan County, Zhejiang Province, China, which
is described elsewhere (9). Simultaneously, a face-to-face
questionnaire was completed, including demographic data and
information concerning drinking water source and smoking his-
tory, and other potentially related factors for colorectal cancer. A
total of 64,693 participants (85.3%) responded to the questions.
Questionnaire data were key-entered twice and processed blind
with respect to case/cohort status to avoid bias in coding and
interpretation of the data. Subjects who reported a history of
cancer in the baseline questionnaire (86 individuals, 0.13%) or
who died during the period May 1989 to April 1990 (129 indi-
viduals, 0.20%) were excluded. Furthermore, 13 cohort members
with inconsistent data were excluded from the analysis. To
acquire more information we retained the other 15 subjects
with missing variables. The final total of 64,115 residents were
classified into five cohorts according to their response to the
question ‘What has been your main source of drinking water
over your lifetime (having been drunk for the longest time)?’,
with the potential answers of: municipal water, private well water,
river water, ditch water and mixed water. Mixed water means
mainly river water and ditch water having similar drunken years.
In fact, the municipal water in Jiashan County is groundwater
from below 600–800 m without chlorine disinfection.
Cohort follow-up and outcome data
Cohort members were followed-up for CRC incidence through a
tumor reporting system including a rapid reporting system of
 Drinking water source and colorectal cancer 653

CRC Registry. The report thoroughness for CRC by the two
registrations was documented to be 95.2% (10). Quality control
of the two registrations was performed by a search for cancer
cases through all the hospitals in the region. Through to
December 31, 2000, after 10.6 years and 680,508 person-years
of follow-up, 242 cohort members had developed CRC, includ-
ing 107 (44.2%) cases of colon cancer and 135 (55.8%) cases of
rectal cancer. A case-control study based on the cohort popu-
lation, carried out in July 2002, consequently estimated that the
out-migration rate among the cohort population was <1%
annually, therefore we regarded the cohort as a fixed cohort,
and only considered death as loss to follow-up. A total of 4885
deaths, including 2331 female, 2554 male and one sex missing, in
our cohort were ascertained through the Jiashan County Death
Registration System. This registration system collected the over-
all death cases, including the cause of death, in Jiashan Country.
demographic variables including age, sex, occupation, marital
status and education. Age was divided into 10-year classes (<40,
40–49, 50–59, 60–69, $70); education into illiteracy and liter-
acy; marital status into married and others; occupation into
farmer and others: smoking history into four classes (never,
ex-smoker, light-smoker, heavy-smoker). Person-years were cal-
culated with every cohort member from 1st May 1990 to end-
point. The end-point was considered to be the date of diagnosis
of CRC, the death date from other causes or 1st January 2001,
whichever came first. Relative risks (RRs) were used with 95%
confidence intervals (CIs) to estimate the strength of associ-
ations between the exposure and CRC. Poisson regression
was used to control potential confounders and to attain
crude and adjusted relative risks based on person-years. All
these calculation were carried out on STATA Version 7.0.

Statistical analysis Results

The exposure variable of primary interest was drinking water The distribution of drinking water source and the putative
source. Stepwise Poisson regression was used to control the confounding variables in the cohort at baseline are presented
confounding effects of smoking history and the common in table 1. Most of the cohort members (62.18%) reported

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Table 1 Relationships between drinking water source and demographic variables among population aged 30 years or
over by drinking water source in Jiashan County of China, 1990–2000

Confounding variables Main source of drinking water over lifetime Total Chi-squared

Municipal Surface Well

River Ditch Mixed

Baseline age (years) 2a 8a 1a

..............................................................................................................................
<40 3963 13722 2168 1344 2508 23705 1871.5*
..............................................................................................................................
40–49 1912 10235 1553 1032 1797 16529
..............................................................................................................................
50–59 921 8202 1310 906 1232 12571
..............................................................................................................................
60–69 294 5515 873 771 698 8151
..............................................................................................................................
$70 111 2184 328 335 190 3148
..............................................................................................................................
a a
Sex 1 1
..............................................................................................................................
Male 3940 19011 2448 1952 3200 30951 172.9*
..............................................................................................................................
Female 3262 20855 3384 2437 3224 33162
..............................................................................................................................
Education
..............................................................................................................................
Illiterate 382 16566 2753 1644 2575 23920 3608.6*
..............................................................................................................................
Literate 6821 23300 3479 2745 3850 40195
..............................................................................................................................
Marital status
..............................................................................................................................
Married 6834 35859 5707 3922 5973 58295 231.0*
..............................................................................................................................
Others 369 4007 525 467 452 5820
..............................................................................................................................
Occupation
..............................................................................................................................
Farmer 195 30462 5924 2402 5528 44511 19232.0*
..............................................................................................................................
Others 7008 9404 308 1987 897 19604
..............................................................................................................................
a a a a a
Smoking history 7 7 1 2 2
..............................................................................................................................
Never 3785 21186 3418 3470 3411 34270 165.3*
..............................................................................................................................
Ex-smoker 168 731 102 125 81 1207
..............................................................................................................................
Light-smoker 630 2505 454 244 411 4244
..............................................................................................................................
Heavy smoker 2613 15437 2257 1548 2520 24375
..............................................................................................................................
Total 7203 (11.23) 39866 (62.18) 6232 (9.72) 4389 (6.85) 6425 (10.02) 64115
a: Missing sum according to the variables
*Significant at P < 0.001 (Pearson chi-squared)
654 European Journal of Public Health

using river water as their main source of drinking water and

11.23%, 9.72%, 6.85% and 10.02%, respectively, answered to
drinking municipal groundwater, ditch water, mixed water and
well water. Significant at P < 0.001 with Pearson chi-squared,
all the distribution of age, sex, occupation, education, marital
status and smoking history was imbalance among the five popu-
lations according to the five sources of drinking water. There-
fore, those potential confounding variables were considered in
the following multivariate regression.
Table 2 shows the incidence densities of CRC by different
sources of drinking water. The incidence densities for colon
cancer, rectal cancer and the total CRC were, respectively,
15.72, 19.84 and 35.56 per 100,000 inhabitants. A trend was seen
toward increasing incidence densities of CRC from municipal
groundwater, river water, ditch water, mixed water to well
water in turn as shown by figures of 29.61, 32.67, 33.45,
40.87, 58.67 per 100,000 inhabitants, respectively. When
colon cancer and rectal cancer were considered separately, the
trend of increasing incidence was similar. Interestingly, people
drinking well water have the highest incidence density of CRC,
and particularly rectal cancer, which differs significantly from
those drinking municipal groundwater who have the lowest
1.432–2.854), respectively. When other drinking water sources
were examined, no significant relationship with CRC was found
at the 0.05 signficance level.
Discussion
Previous epidemiological studies on cancer and drinking water
source have found that polluted surface water sources, e.g. river
water and pond water, are risk factors for CRC with obvious
higher incidence density than other drinking water sources (6).
In fact, the real association is due to the water quality, i.e. the
carcinogens in water and the degree of pollution. Pesticide
remains and nitrate pollutants were examined with interest and
taken as having positive correlation to CRC (7–11). Recently,
drinking water chlorination by-products, e.g. chloroform and
carbon tetrachloride, have been reported to be potential carci-
nogens (6,12,13). Kikuchi (14) found an association between
trace element levels in drinking water and the incidence of CRC
in Japan, and reported that the incidence of CRC changed when
the contents of gold, magnesium, selenium, calcium, phos-
phorus, sodium and strontium etc. changed. Hardness levels

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CRC incidence density (P < 0.05). The incidence densities of
colon cancer were also highest in the well and mixed-water
sources groups, but were not significantly different from those
of municipal groundwater at the 0.05 level.
Crude, age-adjusted and multivariate-adjusted RRs for CRC
were next estimated for populations with different drinking
water sources, as presented in table 3. Populations served by
municipal groundwater sources were chosen as the reference
category because the municipal water supply of Jiashan County
is groundwater below 600–800 m without chlorine disinfection
and because groundwater is considered as unpolluted water
(RR ¼ 1.0). The crude, age-adjusted and multivariate-adjusted
RRs were similar when related to the same drinking water
source. After adjusting for the confounding variables, the
risks of well water could be seen to be significantly higher
than those of municipal groundwater on all colon cancer, rectal
cancer and CRC. The relative risks were 1.741 (95% CI 1.001–
3.029), 2.228 (95% CI 1.432–3.466) and 2.022 (95% CI
in Taiwan’s drinking water were thought to relate to rectal
cancer mortality in Yang’s study (15).
In our study, compared with municipal groundwater, the
incidence density of CRC increased from river water, ditch
water, mixed-water to well water in turn. However, well
water was the only one where the relative risks had significant
statistical meaning. Although systematic error in factors other
than drinking water source and the above putative confounding
variables cannot be excluded, the observed increased risk of
CRC from drinking well water is believable and comprehensible.
Under certain circumstances, the quality of well water may be
similar to the quality of surface water, and may also similarly
easily become polluted. At the same time, well water has a very
reduced flow and is far less susceptible to run-off contamination
than river and ditch water. Well water is generally more min-
eralized and contains higher levels of naturally occurring trace
elements and radioactive substances, which may be carcinogenic
e.g. arsenic and selenium (16,17). It should also be noted that

Table 2 Colorectal cancer (CRC) incidence densities per 100,000 of population aged 30 years or above by drinking water
source in Jiashan County of China, 1990–2000

CRC Main source of drinking water over lifetime Total

Municipal ground Surface Well

River Ditch Mixed

Colon cancer
..............................................................................................................................
Sum 12 61 9 10 15 107
..............................................................................................................................
Person-years 77683 422373 65778 46493 68181 680508
..............................................................................................................................
Incidence density (105) 15.45 14.44 13.68 21.51 22.00 15.72
..............................................................................................................................
Rectal cancer
..............................................................................................................................
Sum 11 77 13 9 25 135
..............................................................................................................................
Person-years 77683 422373 65778 46493 68181 680508
..............................................................................................................................
Incidence density (105) 14.16 18.23 19.76 19.36 36.67* 19.84
..............................................................................................................................
Colorectal cancer
..............................................................................................................................
Sum 23 138 22 19 40 242
..............................................................................................................................
Person-years 77683 422373 65778 46493 68181 680508
..............................................................................................................................
Incidence density (105) 29.61 32.67 33.45 40.87 58.67* 35.56
*Significant at P < 0.05: refers to the population served by municipal groundwater (Poisson regression with one factor)
 Drinking water source and colorectal cancer 655

Table 3 Relative risks (RRs) of colorectal cancer (CRC) in relation to drinking water source among population aged 30 years
or above in Jiashan County of China

RRs of CRC Main source of drinking water over lifetime

Municipal Surface Well

ground
River Ditch Mixed

Colon cancer
..............................................................................................................................
Crude RR (95% CI) 1.000 0.942 (0.508–1.750) 0.893 (0.376–2.120) 1.412 (0.610–3.269) 1.438 (0.673–3.071)
..............................................................................................................................
Age-adjusted RR (95% CI) 1.000 0.645 (0.345–1.210) 0.611 (0.256–1.460) 0.891 (0.381–2.084) 1.098 (0.512–2.356)
..............................................................................................................................
Multivariate RR (95% CI) 1.000 0.881 (0.564–1.377) 1.001 (0.498–2.036) 1.206 (0.621–2.342) 1.741 (1.001–3.029)*
..............................................................................................................................
Rectal cancer
..............................................................................................................................
Crude RR (95% CI) 1.000 1.298 (0.690–2.441) 1.407 (0.630–3.141) 1.386 (0.575–3.346) 2.612 (1.285–5.307)*
..............................................................................................................................
Age-adjusted RR (95% CI) 1.000 0.984 (0.520–1.862) 1.066 (0.475–2.391) 1.000 (0.411–2.429) 2.115 (1.037–4.310)*
..............................................................................................................................
Multivariate RR (95% CI) 1.000 0.986 (0.648–1.500) 1.169 (0.647–2.113) 0.961 (0.484–1.908) 2.228 (1.432–3.466)*
..............................................................................................................................
Colorectal cancer
..............................................................................................................................

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Crude RR (95% CI) 1.000 1.112 (0.715–1.729) 1.139 (0.635–2.043) 1.400 (0.762–2.570) 1.998 (1.196–3.337)*
..............................................................................................................................
Age-adjusted RR (95% CI) 1.000 0.807 (0.516–1.262) 0.826 (0.458–1.488) 0.953 (0.516–1.760) 1.578 (0.943–2.642)
..............................................................................................................................
Multivariate RR (95% CI) 1.000 1.006 (0.613–1.649) 1.106 (0.576–2.124) 1.091 (0.581–2.046) 2.022 (1.432–2.854)*
Multivariate RRs were adjusted for age, sex, education, occupation, marital status and past smoking history, which was
significant at P < 0.05 in stepwise Poisson. The significances of the maximum likelihood ratio chi-squared test of fit for the
afore-cited multivariate Poisson regressions were all extremely close to 1.0 (P ¼ 0.999)
*Significant at P < 0.05 (Poisson regression)

Jiashan County is an agricultural district and, since chemical

fertilizer and pesticide were abused in the middle of 20th century,
organic phosphorus and organic chlorine in particular, which
degrade slowly, may remain in high concentrations in well
water, particularly well water at mid-depth.
The finding that populations drinking surface and well water
have higher rectal cancer and colon cancer risk than those using
municipal groundwater as a drinking source is consistent with
results from other investigations (6,18,19). When cancer sites
are considered in this study the higher risk of rectal cancer
in those drinking well water was statistically significant when
considering either one factor analysis, age-adjusted analysis or
multivariate analysis. While for colon cancer, the association
with well water source was statistically significant only after
adjusting for age, sex, occupation, marital status, education
and smoking history.
Finally, some limitations of this study need to be discussed
when interpreting the results. Some misclassification of
exposure may have occurred, since the exposure status for
study participants was determined via the questionnaire at
the 1989 screening, many members might have subsequently
changed their source of drinking water. However, it is likely
that, in general any change would have been towards using
municipal groundwater, which we considered to be unpolluted
water and used as the reference in our study. Hence, the sys-
tematic bias is simple and the RR may be underestimated, which
could not create a spurious association. One noteworthy prob-
lem in the study is the systematic variation in 11 years’ follow-
up, as was demonstrated in the present study. There may be
some under-reporting in CRC Registration and Death Registra-
tion, which would influence the outcome of follow-up.
Acknowledgement
This work was supported by the National Nature Scientific
Foundation of China (No: 30170828).
Key points
 Study-question: Whether there is the association of
drinking water sources and colorectal cancer incid-
ences, and what kind of drinking water source has
the highest risk for colorectal cancer?
 Main results: Drinking well water over a long period
was identified as playing a role in the risk for CRC,
especially for rectal cancer.
 Implications of the study for public health practice or
policy: It is necessary to control the water pollution,
especially the well water, and farther more enhance the
safe of the drinking water source.
References
1 Young-In K. Diet, lifestyle, and colorectal cancer: Is hyperinsulinemia the
missing link? Nutr Rev 1998;56:275–9.
2 Li LD, Rao KQ. An analysis of cancer incidence and death register
data in 1988–1992, in 11 counties, China. Bull Chinese Cancer
2000;9:435–47.
3 Page T, Harris RH, Epstein SS. Drinking water and cancer mortality in
Louisiana. Science 1976;193:55–7.
4 Griffith J, Riggan WB. Cancer mortality in US counties with hazardous
waste sites and ground water pollution. Arch Environ Health 1989;
44:69–74.
5 Gulis G, Fitz O, Wittgruber J, Suchanova G. Colorectal cancer and
environmental pollution. Cen Eur J Public Health 1998;6:188–91.
6 Doyle TJ, Zheng W, Cerhan JR et al. The association of drinking water
source and chlorination by-products with cancer incidence among
postmenopausal women in Iowa: A prospective cohort study.
Am J Public Health 1997;87:1168–76.
7 Weyer PJ, Cerhan JR, Kross BC et al. Municipal drinking water nitrate level
and cancer risk in older women: the Iowa Women’s Health Study.
Epidemiology 2001;12:327–38.
 656 European Journal of Public Health
8 Van-Leeuwen JA, Walter-Toews D, Abernathy T, Smit B, Shoukri M.
Associations between stomach cancer incidence and drinking water
contamination with atrazine and nitrate in Ontario (Canada)
agroecosystems, 1987–1991. Int J Epidemiol 1999;28:836–40.
9 Chen K, Cai J, Liu XY, Ma XY, Yao KY, Zheng S. Nested case-control
study on the risk factors of colorectal cancer. World J Gastroenterol
2003;9:99–103.
10 Ma XY, Yao KY. A investigation of report quality and fail to report rate
of cancer register system in Jiaoshan county. Zhejiang J Prevent Med
2002;14:19–20.
11 Gulis G, Czompolyova M, Cerhan JR. An ecologic study of nitrate in
municipal drinking water and cancer incidence in Trnava District, Slovakia.
Environ Res 2002;88:182–7.
12 Brennan RJ, Schiestl RH. Chloroform and carbon tetrachloride induce
intrachromosomal recombination and oxidative free radicals in
Saccharomyces cerevisiae. Muta Res 1998;397:271–8.
13 Backer LC, Ashley DL, Bonin MA et al. Household exposures to drinking
water disinfection by-products: whole blood trihalomethane levels. J Expos
Anat Environ Epidemiol. 2000;10:321–6.
View publication stats
14 Kikuchi H, Iwane S, Munakata A, Tamura K, Nakaji S, Sugawara K. Trace
element levels in drinking water and the incidence of colorectal cancer.
Tohoku J Exp Med 1999;188:217–25.
15 Yang CY, Tsai SS, Lai TC, Hung CF, Chiu HF. Rectal cancer mortality
and total hardness levels in Taiwan’s drinking water. Environ Res
1999;80:311–6.
16 Chiou HY, Chiou ST, Hsu YH et al. Incidence of transitional cell carcinoma
and arsenic in drinking water: a follow-up study of 8,102 residents in an
arseniasis-endemic area in northeastern Taiwan. Am J Epidemiol
2001;153:411–8.
17 Vinceti M, Nacci G, Rocchi E et al. Mortality in a population with long-term
exposure to inorganic selenium via drinking water. J Clin Epidemiol
2000;53:1062–8.
18 Bean JA, Isacson P, Hausler WJ, Kohler J. Drinking water and cancer
insidence in iowa. Am J Epidemiol 1982;116:912–22.
19 Gottlieb MS, Carr JK, Morris DT. Cancer and drinking water in louisiana:
colon and rectum. Int J Epidemiol 1981;10:117–25.
Received 9 January 2004, accepted 11 May 2004
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