Helicobacter pylori infection in Kazakhstan: effect of water source and household hygiene.

Abstract

The epidemiology of Helicobacter pylori infection and risk factors associated with its transmission are not well understood. Kazakhstan is country with two ethnic groups, Asian (Kazakhs) and Western (Russians), living under similar socioeconomic conditions. The aim of this study was to examine the seroepidemiologic pattern of H. pylori and hepatitis A among the same individuals from both ethnic groups, with emphasis on water source and household sanitation practices. This was a cross-sectional seroepidemiologic study conducted among unrelated healthy individuals in Kazakhstan. From May through August 1999, individuals between the ages of 10 and 60 years from Almaty, Kazakhstan, were invited to participate. Demographic information, socioeconomic factors, living conditions, and various aspects of the local household environment including access to water were collected. A clean water index (CWI) was created based on combined factors, consistency of boiling water before drinking, frequency of storing and reusing water, and frequency of bathing and showering. H. pylori and hepatitis A antibodies were assessed by enzyme-linked immunosorbent assay. Two hundred eighty-eight individuals between the ages of 10 and 60 years participated. The prevalence of H. pylori infection was almost identical among the two ethnic groups (Russians 79% and Kazakhs 80%). H. pylori infection was inversely correlated with the CWI (i.e., 56%, 79%, and 95% for high, middle, and low, respectively (P < .05). Drinking river water had highest risk of H. pylori infection (OR = 13.6, 95% CI = 1.8-102.4; P < .01, compared with tap water). Crowding showed no significant effect on H. pylori prevalence. Anti-HAV antibodies were found in 86% of the population, 90% among the Russians versus 82% among the Kazakhs (OR = 1.8, 95% CI = 1.1-3.8, P = .05). Although the two infections were highly correlated (P < .001), antibody to both infections were present simultaneously in only 74%. The prevalence of H. pylori infection in Kazakhstan is very high. The data suggest that transmission of H. pylori can be water borne, related to poor sanitary practices, or both. The high prevalence of antibodies to H. pylori and HAV among this population is a marker for poor sanitation and hygienic practices. Reducing the rate of H. pylori transmission will require improvements in overall sanitation including clean water, waste disposal, as well as in household hygienic practices.

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HELICOBACTER PYLORI INFECTION IN KAZAKHSTAN: EFFECT OF WATER
SOURCE AND HOUSEHOLD HYGIENE
ZHANNAT Z. NURGALIEVA, HODA M. MALATY, DAVID Y. GRAHAM, R. ALMUCHAMBETOVA,
A. MACHMUDOVA, D. KAPSULTANOVA, MICHAEL S. OSATO, F. BLAINE HOLLINGER, AND ABAI ZHANGABYLOV
Department of Faculty Therapy, Almaty State Medical University, Almaty, Kazakhstan; Department of Medicine VA Medical Center;
Baylor College of Medicine and Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas
Abstract.
well understood. Kazakhstan is country with two ethnic groups, Asian (Kazakhs) and Western (Russians), living under
similar socioeconomic conditions. The aim of this study was to examine the seroepidemiologic pattern of H. pylori and
hepatitis A among the same individuals from both ethnic groups, with emphasis on water source and household
sanitation practices. This was a cross-sectional seroepidemiologic study conducted among unrelated healthy individ-
uals in Kazakhstan. From May through August 1999, individuals between the ages of 10 and 60 years from Almaty,
Kazakhstan, were invited to participate. Demographic information, socioeconomic factors, living conditions, and various
aspects of the local household environment including access to water were collected. A clean water index (CWI) was
created based on combined factors, consistency of boiling water before drinking, frequency of storing and reusing water,
and frequency of bathing and showering. H. pylori and hepatitis A antibodies were assessed by enzyme-linked immu-
nosorbent assay. Two hundred eighty-eight individuals between the ages of 10 and 60 years participated. The prevalence
of H. pylori infection was almost identical among the two ethnic groups (Russians 79% and Kazakhs 80%). H. pylori
infection was inversely correlated with the CWI (i.e., 56%, 79%, and 95% for high, middle, and low, respectively (P <
.05). Drinking river water had highest risk of H. pylori infection (OR ? 13.6, 95% CI ? 1.8– 102.4; P < .01, compared
with tap water). Crowding showed no significant effect on H. pylori prevalence. Anti-HAV antibodies were found in
86% of the population, 90% among the Russians versus 82% among the Kazakhs (OR ? 1.8, 95% CI ? 1.1–3.8, P ?
.05). Although the two infections were highly correlated (P < .001), antibody to both infections were present simulta-
neously in only 74%. The prevalence of H. pylori infection in Kazakhstan is very high. The data suggest that transmission
of H. pylori can be water borne, related to poor sanitary practices, or both. The high prevalence of antibodies to H. pylori
and HAV among this population is a marker for poor sanitation and hygienic practices. Reducing the rate of H. pylori
transmission will require improvements in overall sanitation including clean water, waste disposal, as well as in house-
hold hygienic practices.
The epidemiology of Helicobacter pylori infection and risk factors associated with its transmission are not
INTRODUCTION
Helicobacter pylori infection has been etiologically associ-
ated with gastritis and the gastritis-associated diseases, peptic
ulcer, gastric adenocarcinoma, and primary gastric lym-
phoma.1The prevalence of H. pylori infection varies both
among and within populations and is inversely related to stan-
dards of living and sanitary practice.2The increased risk of
acquisition of the infection is especially high among those
living in developing countries.3–7The risk is multifactorial
that may include interaction with potentially contaminated
environmental sources as local drinking water, swimming in
rivers, and the ingestion of fecally contaminated vegetables
have all been reported as risk factors for the acquisition of H.
pylori infection.8–14In addition, H. pylori has been reported
to be able to survive in water.15,16
In Kazakhstan, the morbidity and mortality associated with
complications of gastrointestinal diseases is high with gastric
cancer being the second leading cause of cancer death.17Ka-
zakhstan is a large country with a dry harsh climate that is
very cold in the winter and hot in the summer. In many vil-
lages, water is obtained from shallow wells.18Because of the
harsh climate, these wells are typically placed near the house
and the outdoor toilet. It is also unusual for the walls of these
wells to be sealed above the surface to prevent pollution from
the surface.
Kazakhstan has two major ethnic groups, one Asian in ori-
gin, Kazakhs (who trace their origins back to Gengus Khan)
and the other Western, ethnic Russians. Each constitutes ap-
proximately 40% of the population. The fact that different
ethnic groups share similar living and socioeconomic condi-
tions in a region with a high rate of gastric cancer provided an
opportunity to investigate H. pylori infection in these com-
munities. We conducted a cross-sectional study in Kazakhstan
to examine the epidemiology and the risk factors of H. pylori
infection with particular emphasis on the possible relation of
H. pylori infection with water source and household sanita-
tion practices.
MATERIALS AND METHODS
Study population. A cross-sectional seroepidemiologic
study was carried out among unrelated Russian or Kazakh
individuals born in Kazakhstan. The study population con-
sisted primarily of adults who visited Almaty City Emergency
Hospital in Almaty, Kazakhstan (one of the Hospital Affili-
ations of Kazakh State Medical University) for routine health
examinations. In addition, individuals responding to flyers de-
scribing the study were also included. Individuals with upper
gastrointestinal tract symptoms, current clinical evidence or
history of peptic ulcer disease, gastric cancer, gastrointestinal
surgery within 2 months prior to the visit were excluded.
Those who used antacids, antibiotics, or H2-receptor antago-
nists were also excluded. Qualifying individuals were invited
to participate and the overall response was 90%. The study
started in May 1999 and ended in August 1999. Informed
consent was obtained from all human adult participants and
from participants, minors as well as from their parents or legal
guardians. An attempt was made to obtain an equal number
of volunteers per decade from each of the two major ethnic
groups.
Questionnaire. A trained physician interviewed each
volunteer and completed a detailed questionnaire. The indi-
Am. J. Trop. Med. Hyg., 67(2), 2002, pp. 201–206
Copyright © 2002 by The American Society of Tropical Medicine and Hygiene
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viduals were questioned regarding the presence and the fre-
quency of symptoms referable to the upper gastrointestinal
tract including indigestion, heartburn, and sour stomach. De-
mographic data focused on the environment during the sub-
ject’s childhood and included social and economic data (par-
ent’s education and occupation, family income) as well as
living conditions (type of dwelling, number of rooms, number
of persons residing in the home).
Household hygiene questions concerned the water source
used for drinking, cooking, and bathing (i.e., tap, well, or
river), excreta disposal facilities (indoors or outdoors), and
other sanitation practices. When the water supply was a well
or river, questions were asked regarding the distance to the
water source, the type of container used to transport the wa-
ter (e.g., metal or plastic), and whether the container was
covered or uncovered during delivery and storage. The data
about frequency and volume per delivery and the number of
family members were used to estimate the volume of water
available per person per day. Sanitation practices questions
included details about frequency of bathing in the summer
and winter, reuse of water, swimming in rivers, and boiling of
water before drinking. We also assessed the level of exposure
to fecal material in relation to the type of toilet.
Serologic Methods. Each volunteer provided a blood
sample. Sera were stored at −20 C until analyzed. Evaluation
of IgG antibody to the high-molecular-weight cell-associated
proteins of H. pylori was determined using a well-
characterized enzyme-linked immunosorbent assay (HM-
CAP IgG ELISA, Enteric Products, Inc.; Stonybrook, N.Y.).
This ELISA measured IgG antibodies to H. pylori infection.
H. pylori–specific IgG antibodies indicate current or recently
cured infection. The results were interpreted according to the
manufacturer’s instructions. H. pylori infection was defined as
a positive ELISA result.
Serum samples also were tested by enzyme immunoassay
for the qualitative detection of total antibody to hepatitis A
virus (HAVAB EIA, Abbott Laboratories, Diagnostic Divi-
sion; Abbott Park Ill.). The interpretation of the results was
done according to the manufacturer’s instructions.
Methods of Analysis. A clean water index (CWI) was
created on the basis of household sanitation practices re-
lated to water use. Categorization was based on a combina-
tion of three factors (consistency of boiling water before
drinking, frequency of restoring and reusing water, and fre-
quency of bathing and showering) (Table 1). Three levels
were identified ranging from high to low. Water volume used/
household/week was calculated by multiplying the total num-
ber of liters delivered each time. As indicated previously, this
took into account the number of members comprising a
household.
The density or crowding in the home was assessed using a
crowding index defined as the total number of family mem-
bers in the home divided by the total number of rooms in the
home. The crowding index was scored as low (scores 0–1),
moderate (scores 2–3), or high (score > 3).
Categorization of socioeconomic class was based on the
occupation and education of parents using a modification of
the Hollingshead index.19Four educational levels and five
occupational categories were used to identify socioeconomic
conditions. Three socioeconomic statuses were identified: up-
per, middle, and lower. The scale was applied to determine
the socioeconomic status of adults as well as the children’s
parents.
The Mantel-Haenszel X2test was used to assess the asso-
ciations between each independent factor of the study and the
prevalence of H. pylori infection. Univariate and multivariate
analyses, ORs, and 95% CI were calculated for H. pylori
seropositivity associated with the study variables. Risk factors
that were significant in the univariate analysis were used in
the multiple logistic regression models. These models help to
assess the relative importance of H. pylori risk factors while
controlling for other risk factors. The data were analyzed by
using the SAS program (SAS Institute; Cary, N. Car.).
RESULTS
Prevalence of H. pylori infection. A total of 288 volunteers
(233 adults and 55 adolescents and children) participated in
the study (Table 2). Adults ranged in age from 20 to > 60
years and children or adolescents from 10 to 19 years. The
overall prevalence of H. pylori seropositivity was 86% among
adults and 64% among children. By age 20, H. pylori sero-
positivity was 77% increasing to 100% at ages 60 and older.
There was no significant difference in the overall prevalence
of H. pylori infection between males and females (P > .5) or
between the Russians and Kazakhs (P > .5) (Figure 1). Those
who grew up in villages had a higher prevalence of H. pylori
infection than those who grew up in a city (86%. versus 67%,
P < .05) (OR ? 3.1, 95% CI ? 1.7–5.5) (Table 2).
Effect of water source and water-related variables on H.
pylori infection. The prevalence of H. pylori infection was
inversely correlated with the CWI. The infection was signifi-
cantly lower among subjects with the highest CWI (56%)
compared with those with middle (79%) or low (95%) CWI
(P < .05). When the population was stratified by the place of
residence, the general pattern remained among people resid-
ing in cities. Among those living in the villages, the prevalence
of H. pylori was significantly higher among people with the
lowest CWI (95%) than among those with middle (80%) or
high (79%) CWI (P < .01). (Table 3).
The source of drinking water had a strong effect on the
prevalence of H. pylori infection. The prevalence of infection
among river water drinkers was 97% compared with 71%
among those who drank tap water (OR ? 13.6; 95% CI ?
TABLE 1
Variables used in calculating the clean water index
Clean water indexBoiling water before drinking Storing and reusing waterFrequency of bathing and showering
High Consistently boiling water before
drinking
Sometimes boiling water before
drinking
Never boiling water before drinking
Never storing or reusing water At least 2–3 times/week
MiddleSometimes storing and reusing water Less than 2–3 but more than once/week
Low Always storing and reusing water Once/week or less
NURGALIEVA AND OTHERS
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1.8–102, P < .01) (Table 2). Therefore, we examined the effect
of the source of drinking water on the frequency of H. pylori
antibodies in relation to the CWI (Table 4). While the trend
of H. pylori prevalence in relation to the three categories of
the CWI was consistent among those who drank tap or well
water, the rate of infection was high among river water users
irrespective of the CWI category.
The volume of water delivered per household did not have
any effect on the prevalence of H. pylori infection. Boiling
water is a method of disinfection used in many developing
countries and also a marker of household hygienic practices.
In cities, the prevalence of H. pylori among those who used
tap water and consistently boiled water before drinking was
markedly less (38%) than among those who sometimes
(73%), or never (91%) boiled water P ? < .001). Swimming
in rivers was also a risk factor: 86% (143/166) of those who
often swam in rivers were H. pylori infected compared with
67% (65/97) of those who sometimes or never swam in rivers
(P < .001). The difference in H. pylori prevalence in relation
to swimming remained significant even after adjusting for so-
cioeconomic status.
Household sanitary and socioeconomic indicators in rela-
tion to the prevalence of H. pylori infection. The crowding
index showed no significant effect on the prevalence of H.
pylori infection among the populations studied (Table 2). The
relationship of H. pylori prevalence to the use of an outdoor
or indoor toilet was examined as an indicator of household
sanitation practices. H. pylori infection was significantly more
common among those who used outdoor facilities compared
with those who used indoor facilities (crude OR ? 4.5; 95%
CI ? 2.3–8.7). The magnitude of the OR was not reduced by
adjustment for age and socioeconomic variables.
H. pylori prevalence was inversely correlated to socioeco-
nomic status. Those living in a household in which the edu-
cational and occupational levels were low had a higher rate of
H. pylori infection (90%) compared with those from an upper
socioeconomic group (69%) (P < .001). That difference re-
mained significant after adjusting for age. The associations
TABLE 2
Distribution of H. pylori (Hp) infection according to the study variables among 288 Russians and Kazakhs
Variable
Total
no.
(+Hp)
%
Crude
OR 95%CI†
Age & SES*
OR
- Adjusted
95% CI†
Age
10–19
20–29
30–39
40–49
50–59
60–69
SES*
Upper
Middle
Lower
Gender
Male
Female
Ethnicity
Russian
Kazakh
Place where growing up
City
Village
Source of drinking water:
Tap
Well
River
Clean Water Index
Highest
Middle
Lowest
Water volume
Large
Moderate
Small
Toilet inside the home
Yes
No
Crowding Index†
Low
Moderate
High
55
60
52
60
53
64
77
77
83
94
1.0 (Reference)
1.9
1.9
2.9
9.5
9.1
0.8–4.2
0.8–4.4
1.2–6.8
2.6–34.5
0.6–438 100
120
52
116
69
81
90
1.0 (Reference)
1.9
3.9
0.9–41
2.0–7.9
132
156
79
80
1.0 (Reference)
1.1
1.0 (Reference)
1.0 0.6–1.90.6–1.7
135
153
79
80
1.0 (Reference)
1.1
1.0 (Reference)
1.20.7–1.9 0.6–2.1
100
188
67
86
1.0 (Reference)
3.1
1.0 (Reference)
2.01.7–5.5 1.3–3.2
171
78
34
71
90
97
1.0 (Reference)
3.6
13.6
1.0 (Reference)
2.1
5.1
1.6–8.1
1.8–102.4
1.3–2.5
1.8–20.5
50
137
94
56
79
95
1.0 (Reference)
2.9
14.0
1.0 (Reference)
1.9
4.7
1.5–5.8
4.8–40
1.3–3.1
2.3–11.0
13
30
92
92
100
90
1.0 (Reference)
2.5
0.8
1.0 (Reference)
1.8
0.6
0.1–43
0.1–6.6
−0.5–5.7
0.2–2.5
147
141
69
91
1.0 (Reference)
4.5
1.0 (Reference)
2.12.3–8.71.4–4.5
81
128
79
82
77
82
1.0 (Reference)
0.7
1.1
1.0 (Reference)
0.8
1.3
0.4–1.5
0.5–2.4
0.6–1.8
0.7–3.0
* Socioeconomic status
† Crowding Index ? Total number of family members who live in the house Low:
Total # of rooms in the house
< 2
Moderate: 2–3
High: > 3
Water Volume ? Number of liters delivered each trip 10–15 liters/week
20–40 liters/week
> 40 liters/week
H. PYLORI AND HOUSEHOLD SANITATION
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between socioeconomic status, CWI, and H. pylori infection
rates are shown in Figure 2. The lowest prevalence of H.
pylori infection was found in persons from the upper socio-
economic group who had high CWI (39%). However, even
within the upper socioeconomic group there was an inverse
relationship between H. pylori positivity and the CWI (39%,
77%, and 87% for those with high, middle, and low CWI,
respectively) (P < .001).
Hepatitis A serology. Overall, anti-HAV was found in
86% of the population, 90% among the Russians versus 82%
among the Kazakhs (OR ? 1.8, 95% CI ? 1.1–3.8, P ? .05).
Although the two infections were highly correlated (P < .001),
antibody to both infections were present simultaneously in
only 74% (95% CI ? 68–78%) consistent with the concept
that the prevalence of either infection reflects the general
level of sanitation.
DISCUSSION
This is the first study to report the epidemiology of H.
pylori in the newly independent republic of Kazakhstan (a
former part of the Soviet Union). The prevalence of H. pylori
infection was high and did not differ between the two major
ethnic groups, Kazakhs and Russians. One of the most
marked findings of the study was the association between the
prevalence of H. pylori infection and the water use (e.g.,
CWI). The CWI provides a simple measure of household
hygiene. For example, those individuals who consistently
boiled water before drinking and who frequently bathed and
never reused water, had the lowest prevalence of H. pylori.
Socioeconomic status is often a surrogate marker for the level
of sanitary and hygienic practices, and it is a major variable
that frequently correlates with the variation in the prevalence
of H. pylori infection between different races and ethnic
groups. However, in Kazakhstan socioeconomic levels do not
differ markedly and other measures of household hygiene,
such as the CWI, provide a better estimate of the risk of
acquiring H. pylori infections. Although there was an inverse
association between socioeconomic status and H. pylori in-
fection in the current study, socioeconomic status appeared to
be less important than the CWI. This finding is consistent with
a study from Peru that reported that water source was more
important than socioeconomic status for H. pylori acquisi-
tion.11
Excreta disposal is another factor related to household hy-
giene. We found that 91% of those who used outdoor facili-
ties were H. pylori infected compared with 69% of those with
indoor toilets (OR ? 4.5; 95% CI ? 2.3–8.7). Although in-
door toilet facilities for adults may be available in many pro-
vincial villages in Kazakhstan, the feces of infants may be
disposed in the environment near the home (i.e., in places
readily accessible to animals or children). It has been noted
previously that the presence of fecal material near the home
is a risk factor for diarrheal disease.20It is also possible that
good household hygienic practices are compromised in
Kazakhstan villages where the inhabitants must use outdoor
facilities in subzero weather.
Crowding is another indirect measure of household hy-
giene. Although crowding has been reported to be an impor-
tant risk factor for H. pylori acquisition,21–26we did not dem-
onstrate that effect in our study. This is consistent with the
notion that the most important factors influencing transmis-
sion of an infection may differ among ethnic groups and cul-
tures due to differences of the household hygiene practices.
Another major finding of the current study is the higher
TABLE 3
Frequency of H. pylori antibodies among city and village population
according to the clean water index
Water clean index
HighMiddle Low
Variable
City
Village
Total
No./ (% Pos)
22 (27)
28 (79)
50 (56)
No./ (% Pos)
67 (78)
70 (80)
137 (79)
No./ (% Pos)
9 (89)
85 (95)
94 (95)
P Value*
<.001
<.01
<.001
* P value represents the statistical difference between the three clean water index catego-
ries within the city and village population, respectively.
* P value was based on Mantel-Haenszel X2test
TABLE 4
Frequency of H. pylori infection in relation to the source of drinking water and the clean water index
Water clean index
High MiddleLow
Source of drinking water
Tap water (N ? 166)
Well water (N ? 77)
River water (N ? 33)
Total (p for trend)
* P value was based on Mantel-Haenszel X2test
No./ (% Pos)
32 (40)
9 (67)
9 (100)
50 (0.005)
No./ (% Pos)
111 (77)
10 (80)
16 (94)
137 (0.30)
No./ (% Pos)
23 (91)
58 (62)
8 (100)
89 (0.64)
P for trend*
.002
.02
.6
FIGURE 1.
ethnic groups, Russian and Kazakh, individuals born in Kazakhstan
in relation to the age group.
The prevalence of H. pylori infection in the two major
NURGALIEVA AND OTHERS
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prevalence of H. pylori infection among those who used river
water or well water for drinking compared with those who
used tap water. The prevalence of H. pylori infection among
those who used river water as the source of their drinking
water was consistently high regardless of socioeconomic sta-
tus. While studies from the United States, Canada, Japan, and
Sweden have suggested that H. pylori may be present in sur-
face or groundwater,13,14,27,28there was no association found
between H. pylori prevalence and water source, possibly be-
cause of high quality of water treatment.29–31For example,
the study from Bangladesh found no association between H.
pylori prevalence and the use of tube wells, which had been
previously linked to diarrheal disease.32In that population,
H. pylori infection was very common before aged 2 and was
associated with the Hindus ethnic group. This is consistent
with the notion that different populations may have different
specific behaviors that compromise household hygiene and
promote transmission of H. pylori infection. A number of
previous studies have reported an association between water
source and H. pylori infection, which is consistent with our
findings. In another example, a study from Ethiopia reported
a high prevalence of H. pylori among those who used well
water compared with those that use river or piped water.33
Shallow wells are known to be vulnerable to contamination
especially if there is improper sealing of the well near the
surface. Even in the United States, 42% of private wells have
been reported to be contaminated by bacteria as shown by an
increase in coliform bacteria.34Swimming in rivers was also
found as a significant risk factor for H. pylori acquisition
irrespective of whether the river was the primary source of
drinking water. A study from Colombia also reported that
swimming in rivers was associated with a high prevalence of
H. pylori infection.9
It was reported that changes in the epidemiology of H.
pylori follow the same time trends as that of hepatitis A and
polio35and that both may reflect changes in the general level
of sanitation. We subsequently showed that there was a gen-
eral relation between the prevalence of anti-HAV and H.
pylori, which was consistent with this hypothesis.4However,
significant differences in the patterns of transmission between
the two infections make it difficult to actually test that hy-
pothesis directly.36Nonetheless, if HAV and H. pylori were
acquired from a common source, one would expect a high
proportion (e.g., at least 90%) of both infections among the
same individuals. The results from our current study show
that the age–specific prevalence of the two infections are par-
allel which is consistent with the notion that both infections
are epidemiologic markers for poor sanitation and hygiene
practices. Only 74% of the population studied had concor-
dant infections, which indicate that a common source or single
mode of transmission for the two infections is unlikely. This
conclusion is consistent with results obtained among children
from border communities between Mexico and the United
States where the moderate association originally observed be-
tween these two infections was weakened after adjustment for
age and socioeconomic status.37In Italy, the seroprevalences
of HAV and H. pylori infections were analyzed in relation to
a number of variables (e.g., density of living, number of sib-
lings, sharing a bed, and other socioeconomic indicators), and
the authors were not able to find any risk factors shared by
both infections.38
In summary, our data suggest that transmission of H. pylori
is largely opportunistic such that it can result from any route
that can deliver the bacterium to the stomach. Enteric infec-
tion related to water can be either water borne (such as chol-
era) or related to poor sanitary practices (water washed). The
data suggest that H. pylori can be transmitted either way, and
that to reduce the rate of transmission, an improvement in
overall sanitation will be required including clean water,
waste disposal, and household hygienic practices.
Acknowledgments: This material is based upon work supported in
part by the Office of Research and Development Medical Research
Service Department of Veterans Affairs and by Public Health Service
grants DK-53659 and DK56338, which funds the Texas Gulf Coast
Digestive Diseases Center. The HM-CAP IgG ELISA kits were a gift
of Enteric Products, Inc.; Stonybrook, N.Y.
Authors’ addresses: Zhannat Z. Nurgalieva, M.D. e-mail:
Zhannatn@bcm.tmc.edu. David Y. Graham, M.D. e-mail:
dgraham@bcm.tmc.edu. Hoda M. Malaty, M.D., Ph.D., e-mail:
hmalaty@bcm.tmc.edu. Michael S. Osato, Ph.D., e-mail:
mosato@bcm.tmc.edu. Rm 3A-320 (111D) VAMC 2002 Holcombe
Blvd., Houston, TX. 77030. Tel: 713-795-0232. Fax: 713-790-1040. F.
Blaine Hollinger, M.D. e-mail: blaineh@bcm.tmc.edu. Department of
Molecular Virology and Microbiology, Baylor College of Medicine,
One Baylor Plaza, Houston, TX 77030. Tel: 713-798-4454. Fax: 713-
798-3490. Roza K. Almuchambetova, M.D., Aigul K. Machmudova,
M.D., Dina Kapsultanova, M.D., Abai K. Zhangabylov, M.D., De-
partment of Faculty Therapy, Almaty State Medical University, Al-
maty, Kazakhstan. Tel: 011-7-3272-63-48-38. Fax: 011-7-3272-50-70-58.
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FIGURE 2.
prevalence of H. pylori is shown in relation to the socioeconomic
status.
The relation between the clean water index and sero-
H. PYLORI AND HOUSEHOLD SANITATION
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