Hindawi Publishing Corporation
Journal of Pathogens
Volume 2013, Article ID 243246, 5 pages
http://dx.doi.org/10.1155/2013/243246

Clinical Study
Seroepidemiology of Helicobacter pylori Infection in
Tepehuanos Aged 15 Years and Older in Durango, Mexico

Cosme Alvarado-Esquivel

Faculty of Medicine and Nutrition, Juárez University of Durango State, Avenida Universidad S/N, 34000 Durango, DGO, Mexico

Correspondence should be addressed to Cosme Alvarado-Esquivel; alvaradocosme@yahoo.com

Received 9 January 2013; Revised 22 February 2013; Accepted 25 February 2013

Academic Editor: Timothy J. Johnson

Copyright © 2013 Cosme Alvarado-Esquivel. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited.

This study aimed to determine the seroepidemiology of Helicobacter pylori infection in Tepehuanos (an indigenous ethnic group
living in rural Mexico). The prevalence of anti-Helicobacter pylori IgG antibodies was examined in 156 Tepehuanos in Durango
State, Mexico, using an enzyme-linked immunoassay. In addition, sociodemographic, clinical, and behavioral characteristics of
Tepehuanos associated with seropositivity were investigated. In total, 103 (66%) of the 156 participants (mean age 31.03 ± 16.71
years) had Helicobacter pylori IgG antibodies. Fifty-four (52.4%) of the 103 seropositive individuals had Helicobacter pylori IgG
antibody levels higher than 100 U/mL. Males and females had comparable seroprevalence of Helicobacter pylori infection and
Helicobacter pylori IgG antibody levels. The seroprevalence was significantly higher in women with pregnancies than those
without this obstetric characteristic. Logistic regression showed that Helicobacter pylori infection was positively associated with
low education (OR = 3.37; 95% CI: 1.13–10.00;𝑃 = 0.02) and laborer occupation (OR = 2.71; 95% CI: 1.14–6.42;𝑃 = 0.02). This is
the first report of seroprevalence and contributing factors for Helicobacter pylori infection in Tepehuanos and of the association of
Helicobacter pylori infection with laborer occupation. Results warrants further research.

1. Introduction

The spiral-shaped and flagellated bacillus Helicobacter pylori
causes infections in humans worldwide [1]. Estimates indicate
that H. pylori is currently infecting approximately one half of
the world’s population [1, 2]. Although most infections with
H. pylori are asymptomatic, a severe gastric disease including
chronic gastritis, peptic ulcer, gastric mucosa-associated
lymphoid tissue lymphoma, and gastric cancer may occur in
some individuals [1–4]. According to the current knowledge,
dissemination of H. pylori might occur from person to person
[5] and by oral-oral or oral-fecal routes [6]. Infections with H,
pylori might also occur by drinking contaminated water [6,
7]. The seroprevalence of H. pylori varies substantially among
countries being significantly higher in developing countries
than in developed countries [8]. The prevalence of infection
also varies among geographical regions and ethnic groups [6].
Very little knowledge about the epidemiology of H. pylori
infection in Mexico exists. There is a lack of information
about H. pylori infection in Tepehuanos (an ethnic group

in northern Mexico). Tepehuanos consist of indigenous
people living mostly in little remote rural communities.
A cross-sectional study was performed to determine the
seroprevalence of anti-H. pylori antibodies in Tepehuanos
in Durango State, Mexico. In addition, sociodemographic,
clinical, and behavioral characteristics associated with H.
pylori seropositivity in Tepehuanos were also investigated.

2. Materials and Methods

2.1. Study Design and Study Population. Through a cross-
sectional study using serum samples from a recent Tox-
oplasma gondii serosurvey [9], 156 Tepehuanos living in
Durango State, Mexico, were studied. In the previous study,
the purpose of sera collection was to determine the seroepi-
demiology of Toxoplasma gondii in Tepehuanos, and sera
were collected from January 2010 to March 2011. Inclusion
criteria for voluntary participation of the subjects were (1)
subjects of Tepehuano ethnicity, (2) 15 years and older, (3) any
gender, (4) any occupation, and (5) any socioeconomic level.

http://dx.doi.org/10.1155/2013/243246


2 Journal of Pathogens

2.2. Sociodemographic, Clinical, and Behavioral Data. Char-
acteristics of the participants were obtained with the aid
of a standardized questionnaire. Sociodemographic data
including age, gender, birth place, residence, educational
level, occupation, and socioeconomic status were obtained
from all participants. Socioeconomic status in Tepehuanos
was ranked by themselves according to their own perception.
Clinical data explored in Tepehuanos included the presence
of any disease, presence or history of gastritis, peptic ulcer,
gastric cancer, and lymphadenopathy. Clinical data was
obtained from the participants, and a diagnosis of diseases
was based on previous medical consultations. Confirmation
of clinical data by means of further diagnostic procedures was
beyond the scope of the present survey. For women, obstetric
data was also recorded. Behavioral data included animal
contacts, foreign travel, consumption of meat, unpasteurized
milk, unwashed raw vegetables or fruits, or untreated water,
frequency of eating away from home (in restaurants or fast
food outlets), contact with soil (gardening or agriculture),
and type of floorings at home.

2.3. Serological Examination for H. pylori Antibodies. Serum
samples were obtained from all participants and kept frozen
at –20∘C until examined. Serum samples were analyzed
through qualitative and quantitative methods for anti-H.
pylori IgG antibodies with a commercially available enzyme
immunoassay kit, that is, “Anti-H. pylori IgG AccuBind
ELISA” (Monobind Inc., Lake Forest, CA). Anti-H. pylori
IgG antibody levels were expressed as units (U)/mL, and a
result greater than 20 U/mL was considered positive. Test was
performed following the instructions of the manufacturer.

2.4. Statistical Analysis. The statistical analysis was per-
formed with the aid of the software Epi Info version 3.5.4
and SPSS version 15.0. For calculation of the sample size
the following values were used: a reference seroprevalence
of 66% [10] as expected frequency of the factor under study,
7000 as the size of population from which the sample was
selected, a worst acceptable result of 58.5%, and a confidence
level of 95%. The result of the calculation was 150 subjects.
The Pearson chi-square test and the Fisher exact test (when
values were less than 5) were used for comparison of the
frequencies among groups. Age among groups was compared
by the Student’s 𝑡-test. Bivariate and multivariate analyses
were used to assess the association between the characteristics
of the subjects and H. pylori seropositivity. As a criterion for
inclusion of variables in the multivariate analysis, variables
with 𝑃 < 0.20 obtained in the bivariate analysis were
considered. Odds ratio (OR) and 95% confidence interval
(CI) were calculated by multivariate analysis using logistic
regression with the Enter method. A 𝑃 value of < 0.05 was
considered statistically significant.

2.5. Ethical Considerations. This study was approved by the
Ethical Committee of the Instituto de Seguridad y Servicios
Sociales de los Trabajadores del Estado in Durango City. Only
archival serum samples and questionnaires from the previous
survey [9] were used in the present study. However, in the

previous survey, the purpose and procedures of the studies
were explained to all participants, and a written informed
consent was obtained from each participant. The previous
survey was approved by an Institutional Ethical Committee.

3. Results

Of the 156 Tepehuanos studied, 103 (66.0%) were positive
and 53 (34%) were negative for H. pylori IgG antibodies.
General sociodemographic characteristics of the 156 Tepe-
huanos studied are shown in Table 1. Most participants were
born in Durango State; their mean age was 31.03 ± 16.71
years (range 15–89 years). The seroprevalence of H. pylori
infection was not influenced by gender, birth place, residence,
or socioeconomic status. In contrast, the seroprevalence of
H. pylori infection varied significantly with age, educational
level, and occupation. Increased seroprevalence in Tepe-
huanos was found in the age groups of 41–50 (100%) and 61–
70 (100%) years old and in those with low education (up to 6
years of education) (82.4%). In addition, laborer Tepehuanos
(employees, construction workers, agriculturists, etc.) had
a significantly (𝑃 = 0.0001) higher seroprevalence than
nonlaborer Tepehuanos (housewives, students, or neither).
Of the 103 H. pylori IgG positive participants, 54 (52.4%) had
IgG levels higher than 100 U/mL, 27 (26.2%) between 51 to
100 U/mL, and 22 (21.4%) from 21 to 50 U/mL. Levels of anti-
H. pylori IgG antibodies were similar in men and women
(𝑃= 0.30).

With respect to clinical data, there were two Tepehuanos
suffering from gastritis, and both were positive for H. pylori
antibodies. One of them has had lymphadenopathy. The
frequency of gastritis in H. pylori seropositive (2/103) and
H. pylori seronegative (0/53) Tepehuanos was similar (𝑃 =
0.43). No cases of peptic ulcer or gastric cancer among
Tepehuanos were found. Ill participants suffered from a
number of diseases including arthritis, back pain, eye dis-
ease, epilepsy, upper respiratory tract infections, and others.
Clinical data was similar among H. pylori positive and H.
pylori negative individuals. In women, the seroprevalence of
H. pylori infection was significantly (𝑃 = 0.02) higher in
women with pregnancies (35/48: 72.9%) than those without
such history (19/38: 50.0%). The seroprevalence of H. pylori
infection was similar (𝑃= 0.60) in pregnant and nonpregnant
women (1/2 and 53/84, resp.). The seroprevalence was similar
in women who have had cesarean sections, deliveries, and
abortions than those without such obstetric characteristics.

Regarding behavioral characteristics, three variables
showed 𝑃 values < 0.20 by bivariate analysis: consumption
of meat (𝑃 = 0.03), frequency of meat consumption (𝑃 =
0.04), and frequency of eating away from home (𝑃 = 0.06).
Other behavioral characteristics including animal contacts,
foreign travel, consumption of unpasteurized milk, unwashed
raw vegetables or fruits, or untreated water, contact with
soil, and type of floorings at home showed 𝑃 values higher
than 0.20 in the bivariate analysis. Table 2 shows the results
of the bivariate analysis of behavioral characteristics and H.
pylori seroprevalence. Further analysis using logistic regres-
sion of sociodemographic and behavioral characteristics of



Journal of Pathogens 3

Table 1: Sociodemographic characteristics of Tepehuanos and seroprevalence of H. pylori infection.

Characteristic No. of subjects testeda Prevalence of H. pylori infection 𝑃value
No. %

Gender
Male 68 48 70.6 0.29
Female 88 55 62.5

Age groups (years)
15–30 98 54 55.1 0.002
31–40 19 16 84.2
41–50 13 13 100.0
51–60 15 11 73.3
61–70 6 6 100.0
71–89 4 2 50.0

Birth place
Durango State 153 102 66.7 0.62
Other Mexican state 2 1 50.0

Residence area
Urban 13 8 61.5 0.74
Rural 141 93 66.0

Educational level
Up to 6 years of education 74 61 82.4 0.00001
7 or more years of education 81 41 50.6

Occupation
Laborerb 68 56 82.4 0.0001
Nonlaborerc 88 47 53.4

Socioeconomic level
Low 147 95 64.6 0.26
Medium 8 7 87.5

aSubjects with available data.
bEmployee, construction worker, business, factory worker, others.
cHousewife, student, or neither.

Tepehuanos showed that H. pylori infection was positively
associated with low education (OR = 3.37; 95% CI: 1.13–10.00;
𝑃 = 0.02) and laborer occupation (OR = 2.71; 95% CI: 1.14–
6.42;𝑃= 0.02) (Table 3).

4. Discussion

The 66% seroprevalence of H. pylori infection found in Tepe-
huanos in Durango, Mexico, is similar to the mean national
seroprevalence (66%) reported in Mexico [10]. However, this
comparison should be interpreted with care, since different
test methods in the studies were used. A commercial ELISA
was used in the present study, while a homemade ELISA was
used in the national survey. The national survey in Mexico
[10] did not provide specific seroprevalence in Durango.
However, the seroprevalence found in Tepehuanos is higher
than a 50.7% seroprevalence found in Mennonites (an ethnic
group of German descent living in rural communities) in
Durango [11]. In both studies in ethnic groups in Durango the
same test (commercial ELISA) was used. In an international
context, the seroprevalence of H. pylori infection in Tepe-
huanos in Durango is lower than the estimated 80%–90%

seroprevalence of H. pylori infection in developing countries
[8].

With respect to the sociodemographic characteristics of
Tepehuanos, seropositivity to H. pylori was found even in the
youngest participants (55.1% in ages of 15–30 years old), and
some older groups (41–50 and 61–70 years old) showed a 100%
seroprevalence of H. pylori infection. The former suggests an
early exposure to H. pylori in the studied population, and
the latter follows a typical increase in the frequency of H.
pylori infection in humans as reported elsewhere [5, 10, 12]. In
the present study, multivariate analysis of sociodemographic
and behavioral characteristics of Tepehuanos showed that
seropositivity to H. pylori was associated with low education
(up to 6 years of education) (OR = 3.37; 95% CI: 1.13–10.00;
𝑃 = 0.02) and laborer occupation (OR = 2.71; 95% CI:
1.14–6.42;𝑃 = 0.02). The finding of an association between
H. pylori infection and low educational level in Tepehuanos
agrees with the data found in the national survey in Mexico
[10]. On the other hand, the finding that laborer Tepehuanos
showed a significantly higher seroprevalence of H. pylori
than nonlaborers is intriguing. The variable age was not
responsible for the difference in the seroprevalence among



4 Journal of Pathogens

Table 2: Bivariate analysis of selected behavioral characteristics of Tepehuanos and seroprevalence of H. pylori infection.

Characteristic No. of subjects testeda Prevalence of H. pylori infection 𝑃value
No. %

Cats at home
Yes 80 52 65 0.78
No 76 51 67.1

Raising animalsb

Yes 130 86 66.2 0.94
No 26 17 65.4

Eating outside home
Never 33 26 78.8 0.06
From 1 to 10 times a year 99 59 59.6
More than 10 times a year 22 17 77.3

Meat consumption
Yes 153 103 67.3 0.03
No 3 0 0

Frequency of meat consumption
Never 3 0 0 0.04
Up to 3 times a week 148 100 67.6
4–7 times a week 4 3 75

Raw cow milk consumption
Yes 106 69 65.1 0.59
No 49 34 69.4

Unwashed raw vegetables
Yes 62 40 64.5 0.67
No 93 63 67.7

Unwashed raw fruits
Yes 85 56 65.9 0.86
No 70 47 67.1

Untreated water
Yes 128 84 65.6 0.63
No 27 19 70.3

Traveled abroad
Yes 7 5 71.4 1
No 149 98 65.8

National trips
Yes 60 42 70 0.38
No 95 60 63.2

Soil contact
Yes 142 95 66.9 0.76
No 13 8 61.5

Floor at home
Ceramic 21 14 66.7 0.73
Concrete 57 40 70.2
Soil 77 49 63.6

aSums may not add up to 156 because of missing values.
bRaising of any kind of animals.

laborer and nonlaborer Tepehuanos, since age adjustment
was included in the multivariate analysis. To my knowledge,
there are not any previous reports of an association of laborer
occupation with H. pylori seropositivity. It is not clear why
laborer Tepehuanos had a higher H. pylori seroprevalence

than nonlaborers. It is possible that laborer Tepehuanos
are in closer contact with the H. pylori source of infection
than nonlaborer Tepehuanos. Other sociodemographic and
behavioral characteristics explored in Tepehuanos were not
associated with H. pylori seropositivity. The socioeconomic



Journal of Pathogens 5

Table 3: Multivariate analysis of selected characteristics of Tepe-
huanos and their association with H. pylori infection.

Characteristic Oddsratio
95% confidence

interval P value

Age 1 0.96–1.03 0.98
Low education 3.37 1.13–10.00 0.02
Laborer 2.71 1.14–6.42 0.02
Eating outside home 0.94 0.46–1.93 0.88
Meat consumption — — 0.99
Frequency of meat
consumption 1.06 0.08–13.15 0.95

status did not influence the seroprevalence of H. pylori
infection in Tepehuanos. This finding conflicts with those
found in other studies [5, 10] where H. pylori infection was
associated with a low socioeconomic status. Consumption of
meat has been associated with a significant increase of anti-
H. pylori IgM antibodies in Kenyan children [13]. In addition,
H. pylori infection has been related with meat consumption
in children in Mexico [14]. However, the associations of H.
pylori seropositivity with meat consumption and frequency
of meat consumption obtained in the bivariate analysis in the
present study did not resist the multivariate analysis. Further
research about the association of H. pylori infection with meat
consumption using a larger sample size population is needed.

Of the clinical characteristics explored, there was no
difference in the frequency of gastritis or other clinical data
among H. pylori positive and H. pylori negative Tepehuanos.
There were only 2 gastritis cases, and both were positive for H.
pylori. Therefore, H. pylori-associated gastritis exists among
Tepehuanos, and further research to evaluate the impact of
H. pylori on the health of Tepehuanos is needed. In the
present study, the seroprevalence of H. pylori infection was
significantly higher in women who have had pregnancies
than those without this obstetric history. This finding agrees
with that found in a study of pregnant women in Israel [15]
where researchers found that women positive for H. pylori
had more prior pregnancies than H. pylori negative women.
The higher seroprevalence of H. pylori infection in women
with pregnancies than those without pregnancies found in
the present study was likely due to difference in age among
the groups. The mean age in women with pregnancies (36.3 ±
14.8 years old) was significantly higher than that (18.6 ± 5.7
years old) in women without pregnancies (𝑃< 0.000001).

This is the first report of seroprevalence and contributing
factors for Helicobacter pylori infection in Tepehuanos and of
the association of Helicobacter pylori infection with laborer
occupation. Results warrants further research.

References

[1] P. Ruggiero, “Helicobacter pylori and inflammation,” Current
Pharmaceutical Design, vol. 16, no. 38, pp. 4225–4236, 2010.

[2] G. Sachs, D. R. Scott, and Y. Wen, “Gastric infection by
Helicobacter pylori,” Current Gastroenterology Reports, vol. 13,
pp. 540–546, 2011.

[3] P. Malfertheiner, “The intriguing relationship of Helicobacter
pylori infection and acid secretion in peptic ulcer disease and
gastric cancer,” Digestive Diseases, vol. 29, pp. 459–464, 2011.

[4] J. Zabaleta, “Multifactorial etiology of gastric cancer,” Methods
in Molecular Biology, vol. 863, pp. 411–435, 2012.

[5] A. C. Ford and A. T. R. Axon, “Epidemiology of Helicobacter
pylori infection and Public Health Implications,” Helicobacter,
vol. 15, no. 1, pp. 1–6, 2010.

[6] K. L. Goh, W. K. Chan, S. Shiota, and Y. Yamaoka, “Epi-
demiology of Helicobacter pylori infection and public health
implications,” Helicobacter, vol. 1, Supplement 1, pp. 1–9, 2011.

[7] D. M. M. Queiroz and F. Luzza, “Epidemiology of Helicobacter
pylori infection,” Helicobacter, vol. 11, Supplement 1, pp. 1–5,
2006.

[8] D. Y. Graham, E. Adam, G. T. Reddy et al., “Seroepidemiology
of Helicobacter pylori infection in India. Comparison of devel-
oping and developed countries,” Digestive Diseases and Sciences,
vol. 36, no. 8, pp. 1084–1088, 1991.

[9] C. Alvarado-Esquivel, S. Estrada-Mart́ınez, L. Garćıa-López
CR, A. Rojas-Rivera, A. Sifuentes-Álvarez, and O. Liesen-
feld, “Seroepidemiology of Toxoplasma gondii infection in
Tepehuanos in Durango, Mexico,” Vector-Borne and Zoonotic
Diseases, vol. 12, pp. 138–142, 2012.

[10] J. Torres, Y. Leal-Herrera, G. Perez-Perez et al., “A community-
based seroepidemiologic study of Helicobacter pylori infection
in Mexico,” Journal of Infectious Diseases, vol. 178, no. 4, pp.
1089–1094, 1998.

[11] C. Alvarado-Esquivel, “Seroepidemiology of Helicobacter pylori
infection in a Mennonite community in Durango State, Mex-
ico,” Helicobacter, 2012.

[12] S. Sasidharan, S. J. T. Lachumy, M. Ravichandran, L. Y. Latha,
and S. R. S. Gegu, “Epidemiology of Helicobacter pylori among
multiracial community in Northern Peninsular, Malaysia: effect
of age across race and gender,” Asian Pacific Journal of Tropical
Medicine, vol. 4, no. 1, pp. 72–75, 2011.

[13] J. H. Siekmann, L. H. Allen, M. R. Watnik et al., “Titers of
antibody to common pathogens: relation to food-based inter-
ventions in rural Kenyan schoolchildren,” American Journal of
Clinical Nutrition, vol. 77, no. 1, pp. 242–249, 2003.

[14] R. Calva-Rodŕıguez, J. J. Luna-Alcántara, B. Lagunes-Yannelli,
M. E. Rivera-Domı́nguez, D. Calva-Cerqueira, and E. Santos-
Marcial, “Prevalence and risk factors of Helicobacter pylori
infection in three populations of children in Puebla, Mexico,”
Revista de Gastroenterologı́a de México, vol. 71, pp. 440–445,
2006.

[15] H. Shirin, O. Sadan, O. Shevah et al., “Positive serology for
Helicobacter pylori and vomiting in the pregnancy,” Archives of
Gynecology and Obstetrics, vol. 270, no. 1, pp. 10–14, 2004.