Am. J. Trop. Med. Hyg., 85(5), 2011, pp. 913–918
Copyright © 2011 by The American Society of Tropical Medicine and Hygiene
Anemia is a serious global health concern that affects one-
quarter of the world’s population and 40% of pre-school–
aged children. 1– 3 It is associated with increased susceptibility
to infection, decreased work productivity, and delayed phys-
ical and cognitive development. 3– 6 In the developing world,
the most common causes of anemia are micronutrient defi-
ciencies, parasitic diseases, and inherited disorders of hemo-
globin. 7 Helicobacter pylori , an inflammatory gastric bacterial
infection especially prevalent in developing countries, 8– 10 has
been implicated as a possible etiology for anemia. 11, 12 Haiti’s
Central Plateau is a particularly impoverished region with a
high prevalence of anemia. 13, 14 Because the identification of
etiological factors would aid anemia interventions, we con-
ducted a cross-sectional study of pediatric and adult subjects
visiting mobile clinics in the rural Central Plateau of Haiti to
estimate the prevalence of anemia and look for associations
with sanitary conditions and H. pylori infection.
Study population. This study was a cross-sectional study
conducted at mobile clinics organized by Project Medishare in
November 2007, 2008, and 2009 in the Central Plateau of Haiti.
In 2007 and 2008, children 6–59 months of age were recruited.
Preliminary analyses found a high prevalence of anemia in these
children, and therefore, in November of 2009, data collection
was expanded to include adult subjects and examine H. pylori
seroreactivities as a potential risk factor for anemia. Project
Medishare is a non-profit organization based in Miami, FL and
Thomonde, Haiti, that shares human and technical resources
between countries to deliver healthcare and development
services to rural Haitian communities. 15 The Institutional
Review Board of Emory University and the Director of the
Ministry of Public Health for the Central Plateau of Haiti
approved the study. Kreyol speaking interpreters informed all
participants of the purpose, procedures, risks, and benefits of
the study, and we obtained written consent from all adults and
from guardians of all subjects less than 18 years of age. No
compensation was provided to the patients for participation
in the study.
A convenience sample of participants was recruited during
4-day free mobile clinics organized by Project Medishare for
Haiti. In 2009, the most common reasons for presentation to
the adult clinic were generalized pain, well-woman check-up,
vision problems, hypertension, and malnutrition. In the same
year, the most common reasons for presentation to the pedi-
atric clinic were intestinal parasites, anemia, rash, and upper
respiratory infection (Leeds I and Zaeh S, unpublished data).
Each mobile clinic took place within the La Hoye area of
the Central Plateau and provided basic medical screening
and treatment, with referrals to local hospitals when neces-
sary. All subjects arriving for care at the mobile clinics were
approached for enrollment. Exclusion criteria included refusal
of consent, presentation with severe medical conditions that
necessitated urgent care, and age less than 6 months. Using
a standard questionnaire, Kreyol-speaking staff conducted
interviews with adult participants and caretakers of minor
participants. Information was collected on village of residence,
number of persons per household, source of drinking water,
water purification practices, and location of defecation. For
children, anthropometric measurements included height or
length using a wooden measuring board accurate to 0.1 cm
(Irwin Shorr Productions, Olney, MD) and weight to the near-
est 0.1 kg using a digital scale (Seca Corp, Hanover, MD).
Laboratory analysis. Non-fasting blood samples were
obtained by finger stick in the sitting position. Hemoglobin
concentrations were measured directly from the finger
using calibrated HemoCue B-Hemoglobin photometer
(Ängelholm, Sweden). H. pylori seroreactivity was measured
using the Quidel Quickvue Rapid Whole Blood Antibody Test
(San Diego, CA) or the PerMaxim RediScreen H. pylori Test
Device (Santa Rosa, CA) according to the manufacturers’
Statistical methods. Data sources for the 6–59 months
subgroup included surveys conducted in 2007–2009, and
measured exposures included sex, age, water source, water
treatment, location of defecation, number in household,
stunting, underweight, wasting, and H. pylori seroreactivity
(2009 only). For this subgroup, age was divided into five
categories: 6–11 months, 12–23 months, 24–35 months, 36–47
months, and 48–59 months. Z scores for height for age/length
Anemia and Helicobacter pylori Seroreactivity in a Rural Haitian Population
Joshua R. Shak ,* Jamie B. Sodikoff , Rebecca A. Speckman , Francois G. Rollin ,
Marie P. Chery , Conrad R. Cole , and Parminder S. Suchdev
Emory University School of Medicine, Atlanta, Georgia; Project Medishare, Thomonde, Haiti
Abstract. Anemia is a significant health concern worldwide and can be the result of nutritional, environmental, social,
and infectious etiologies. We estimated the prevalence of anemia in 336 pre-school children and 132 adults in the rural
Central Plateau of Haiti and assessed associations with age, sex, household size, water source, sanitation, and Helicobacter
pylori seroreactivity using logistic regression analysis; 80.1% (269/336) of children and 63.6% (84/132) of adults were ane-
mic. Among children, younger age was associated with increased prevalence of anemia (adjusted odds ratio [aOR] = 4.1,
95% confidence interval [CI] = 1.5–11.1 for children 6–11 months compared with children 48–59 months). Among adults,
50.8% were H. pylori -seropositive, and seropositivity was inversely associated with anemia (aOR = 0.4, 95% CI = 0.2–0.9).
Anemia prevalence in this region of Haiti is very high and not attributable to sanitary conditions or a high prevalence of
H. pylori infection.
* Address correspondence to Joshua R. Shak, Emory University
School of Medicine, 1648 Pierce Drive, Room 374, Atlanta, GA 30322.
SHAK AND OTHERS
for age (HAZ), weight for age (WAZ), and weight for height/
weight for length (WHZ) were calculated using the 2009 World
Health Organization (WHO) growth standards (Anthro macro
for SAS). Stunting was defined as HAZ < −2, underweight was
defined WAZ < −2, and wasting was defined as WHZ < −2.
Data for the adult subgroup (≥ 16 years) came from the 2009
survey, and exposure variables included sex, age, water source,
water treatment, location of defecation, number in household,
and H. pylori seroreactivity. For this subgroup, age was divided
into categories: 16–24 years, 25–34 years, 35–44 years, 45–54
years, 55–64 years, and ≥ 65 years.
The primary study outcome was anemia. Anemia was
defined according to WHO hemoglobin cutoffs: < 11.0 g/dL
for children 6–59 months, < 12.0 g/dL for women, and <13.0 g/
dL for men. 4 Unadjusted association of exposures with ane-
mia was assessed using χ 2 or Fisher exact tests for contingency
tables. Unadjusted odds ratios with 95% Wald confidence
intervals were obtained using unadjusted logistic regression
models. Adjusted odds ratios were obtained using a multi-
variate logistic regression model for each study group (6–59
months and ≥16 years). Potential confounders of variables
crudely associated with anemia were identified by assessing
crude associations between variables that were considered to
be possible confounders.
Variables that were associated with anemia in the crude
analysis either by statistical significance or meaningful mag-
nitude of association (including potential confounders) and
variables previously shown to be associated with anemia (sex
and anthropometric measures of nutritional status) were
retained in the multivariate models. The multivariate model
for the pediatric group included sex, age, household size,
and malnutrition indicators. A multivariate model including
H. pylori , which was collected only in 2009, was performed on
the 2009 subgroup. The multivariate model for the adult group
included sex, age, and H. pylori . Colinearity among covariates
in the multivariate models was evaluated using linear regres-
sion and was not found to be present. Interaction terms for
sex with other covariates were dropped from the adult mul-
tivariate model by backward elimination. Interaction terms
for study year with other covariates were dropped from the
pediatric multivariate model by backward elimination. In sec-
ondary analyses, linear regression models with hemoglobin as
a continuous outcome and polytomous logistic regression
models with two categories of anemia (mild = hemoglobin
from 9.0 to age- and sex-specific cutoff; moderate to severe =
hemoglobin less than 9.0) as outcomes were evaluated.
Statistical analyses were conducted using SAS version 9.2.
A P value ≤ 0.05 was considered statistically significant.
Children. Of 336 children 6–59 months of age included in
the analysis ( Figure 1A ), 67 (19.9%) were not anemic (Hb ≥
11), 174 (51.8%) were mildly anemic (9 ≤ Hb < 11), 84 (25.0%)
were moderately anemic (7 ≤ Hb < 9), and 11 (3.3%) were
severely anemic (Hb < 7) ( Table 1 ). The mean age of those
children without anemia (32.5 months) was significantly greater
than the mean age of subjects with anemia (25.6 months; P =
0.001). Among children, 250 (74.4%) reported using unpiped
water as their primary drinking source, 97 (28.9%) reported
drinking untreated water, 226 (67.3%) reported regularly
defecating in a bush or on the ground, 119 (35.4%) reported
living in a household with greater than six people, and 4 (8.2%
of 49 subjects tested for H. pylori ) were H. pylori -seropositive
( Table 1 ). In addition, malnutrition was common in children,
with 22.0% stunted, 14.9% underweight, and 6.3% wasted.
There was no meaningful difference in the prevalence of
anemia between male (81.1%) and female (79.1%) children
( P = 0.64) ( Table 2 ). In the unadjusted analysis, children 6–11
months were more likely to be anemic with an unadjusted
Figure 1. Flowcharts of enrollment for pediatric (A) and adult
(B) study groups.
Prevalence of anemia, sanitary conditions, and H. pylori seroreactivity
in pediatric and adult populations
Children 6–59 months
( N = 336)
Adults ≥ 16 years
( N = 132)
n Percent (95% CI) * n Percent (95% CI) *
Mild (> 9.0) †
Severe (< 7.0)
H. pylori positive ‡
More than six in
164 48.8 (43.4, 54.3)
67 19.9 (15.8, 24.6)
269 80.1 (75.4, 84.2)
174 51.8 (46.3, 57.2)
84 25.0 (20.5, 30.0)
113.3 (1.7, 5.8)
48.2 (2.3, 19.6)
74 22.0 (17.7, 26.8) NA
50 14.9 (11.3, 19.1) NA
216.3 (3.9, 9.4)
29.6 (21.9, 38.1)
36.4 (28.2, 45.2)
63.6 (54.8, 71.8)
53.8 (44.9, 62.5)
8.3 (4.2, 14.4)
1.5 (0.2, 5.4)
50.8 (41.9, 59.6)
250 74.4 (69.4, 79.0) 123
97 28.9 (24.1, 34.0)
93.2 (87.5, 96.8)
55.3 (46.4, 64.0) 73
226 67.3 (62.0, 72.3) 7758.3 (49.4, 66.9)
119 35.4 (30.3, 40.8) 5843.9 (35.3, 52.8)
* Exact confidence intervals for proportions.
† Upper cutoff was 11.0 for children, 12.0 for adult females, and 13.0 for adult males.
‡ H. pylori data was collected only for 2009. For children, number is of 49 with H. pylori
values recorded in 2009.
ANEMIA IN A RURAL HAITIAN POPULATION
odds ratio of 4.1 (95% confidence interval [CI] = 1.5–11.1)
compared with children 48–59 months. Subjects 12–23 months
were also more likely to be anemic, but this association was
not statistically significant (odds ratio [OR] = 2.3, 95% CI =
0.9–5.4, P = 0.07). There were no statistically significant dif-
ferences based on sex, water source, water treatment, defeca-
tion location, household size, anthropometric measurements,
H. pylori seropositivity, or study year. In the multivariate analysis,
children 6–11 months and 12–23 months were still more likely
to be anemic than those children 48–59 months, with adjusted
ORs of 4.5 (1.6–12.4) and 2.4 (1.0–5.9, P < 0.05), respectively.
As in the unadjusted models, no variable besides age was sig-
nificantly associated with anemia. In a multivariate regression
model of the 2009 subsample, there remained no statistically
significant association of H. pylori with anemia. Models using
hemoglobin as a continuous outcome or multiple anemia cat-
egories as outcomes did not change the main findings.
Adults. During the 4-day study period in 2009, a total of 225
of 270 persons ≥ 16 years of age were enrolled (enrollment
rate = 83.3%); 93 of these subjects had missing data, leaving
132 subjects in the final analysis ( Figure 1B ). Of those subjects
in the analysis, 48 (36.4%) were not anemic (Hb > 13 for men
and Hb > 12 for women), 71 (53.8%) were mildly anemic
(9 ≤ Hb < upper limit for sex), 11 (8.0%) were moderately
anemic (7 ≤ Hb < 9), and 2 (1.5%) were severely anemic (Hb
< 7) ( Table 1 ). There was no statistically significant difference
between the mean ages of subjects with anemia (43.1 years)
and those subjects without anemia (45.2 years; P = 0.05).
Among adults, 123 (93.2%) reported using unpiped water as
their primary drinking source, 55 (55.3%) reported drinking
untreated water, 77 (58.3%) reported regularly defecating
in a bush or on the ground, 58 (43.9%) reported living in a
household with greater than six people, and 67 (50.8%) were
H. pylori -seropositive ( Table 1 ).
Of 39 males, 24 (61.5%) were anemic compared with 60 of
93 females (64.5%). Sex, water source, water treatment, loca-
tion of defecation, and number in household were not sig-
nificantly associated with anemia in unadjusted or adjusted
analyses ( Table 3 ). Those subjects in the 45–54 year age group
were significantly less likely to be anemic, with an unadjusted
Risk factor frequencies by category and unadjusted and adjusted associations with anemia in 336 pediatric subjects (6–59 months) in 2007–2009
Anemic n (%)
χ2 P value Unadjusted OR (95% CI)Adjusted OR (95% CI)*
Bush or ground
Latrine or toilet
Number in household
≤ 6 (median)
H. pylori rapid test§
0.642 1.14 (0.66, 1.94)
1.20 (0.69, 2.08)
0.016 † 4.12 (1.52, 11.14)‡
2.27 (0.94, 5.43)
1.31 (0.57, 2.99)
1.09 (0.47, 2.51)
4.47 (1.62, 12.35)‡
2.39 (0.98, 5.85)
1.28 (0.55, 2.97)
1.12 (0.48, 2.62)
0.7950.80 (0.41, 1.56)
0.82 (0.37, 1.79)
0.9181.03 (0.57, 1.87)
0.78 (0.44, 1.36)
1.50 (0.83, 2.69)
1.52 (0.83, 2.80)
74 59 (79.7)
0.936 0.97 (0.51, 1.85)
1.18 (0.51, 2.73)
0.9911.00 (0.47, 2.11)
1.05 (0.37, 2.95)
0.9161.06 (0.35, 3.27)
0.81 (0.23, 2.88)
0.431 ¶ 0.75 (0.07, 8.09)
1.15 (0.64, 2.07)
0.96 (0.45, 2.03)
* Adjusted model includes sex, age, number in household, stunted, underweight, and wasted.
† χ 2 P value < 0.05.
‡ Wald P value for category OR < 0.05.
§ H. pylori data collected only for 2009.
¶ Fisher exact test P value.
SHAK AND OTHERS
OR of 0.3 (0.09–0.95) and an adjusted OR of 0.2 (0.07–0.82)
compared with those subjects ≥ 65 years ( P = 0.04) ( Table 3 ).
H. pylori seropositivity was negatively associated with ane-
mia, with an unadjusted OR of 0.5 (95% CI = 0.2–1.0) and
adjusted OR of 0.4 (95% CI = 0.2–0.9) ( Table 3 ). Models
using hemoglobin as a continuous outcome or mild and severe
anemia categories as outcomes did not change the main
The prevalence of anemia in this rural Haitian population
was alarmingly high; four of five children and nearly two of
three adults were anemic. This rate is higher than reported
in other developing countries 3, 17 and higher than reported in
previous surveys of Haiti. In 2005–2006, the Demographic
and Health Surveys (DHS) of Haiti estimated a national 61%
prevalence of anemia in Haitian children 6–59 months, 46%
prevalence of anemia in adult women, and 24% prevalence
of anemia in adult men. 13 Within the Central Plateau region
of Haiti, the DHS reported a 64% prevalence of anemia in
children 6–59 months, a 43% prevalence in adult women, and
a 22% prevalence in adult men. Our finding of higher prev-
alence of anemia in people from the Central Plateau com-
pared with those people reported by the DHS survey could
be attributable to selection bias inherent in our study design;
subjects visiting mobile clinics are presumably less healthy
than the general population. That said, several natural disas-
ters occurring even before the January 2010 earthquake,
including Hurricane Hanna in 2008, may have increased ane-
mia prevalence because of resulting food insecurity, disrup-
tion of existing nutrition programs, and spread of infectious
The higher prevalence of anemia in the 6- to 23-month
group was particularly concerning, because the cognitive
effects of anemia during this period of critical brain develop-
ment may be irreversible. 4, 19 This age group is especially vul-
nerable to anemia because of increased iron metabolism and
the shift from breastfeeding to table foods. 3, 7, 20, 21 A 2004 study
of the nutrient content of traditional complementary table
food in Haiti found inadequate densities of iron, zinc, or vita-
min A. 22 Although we found a high prevalence of malnutrition
and poor sanitation among both the pediatric and adult popu-
lations studied, we did not find an association of anemia with
stunting or wasting. This result contrasts with previous stud-
ies that found associations between severe forms of anemia
and poor growth, 23– 25 and it may implicate a non-nutritional
etiology for anemia in our study population, such as infection,
inflammation, or inherited blood disorders.
Although the prevalence of H. pylori antibodies in adults
was similar to other studies, 26, 27 it was surprising that there was
an inverse association between anemia and H. pylori serore-
activity. This finding contrasts with previous studies that have
reported a positive association. 12, 28 In addition, meta-analyses
of randomized control trials of H. pylori eradication have indi-
cated that eradication can increase hemoglobin levels. 12, 28– 30
However, one study of pregnant women on Pemba Island,
Zanzibar, found a positive association between hemoglobin
concentration and H. pylori bacteria load. 31 Farang and oth-
ers 31 suggest that high bacterial load infection enhances hemo-
globin concentrations by increasing the production of stomach
acid, and low bacterial load infections correspond to advanced
Risk factor frequencies by category and unadjusted and adjusted associations with anemia in 132 adult subjects (≥ 16 years) in 2009
Risk factor n Anemic n (%)
χ 2 P valueUnadjusted OR (95% CI) Adjusted OR (95% CI) *
≥ 65 years
Bush or ground
Latrine or toilet
Number in household
≤ 6 (median)
H. pylori rapid test
0.7460.88 (0.41, 1.91)
0.79 (0.33, 1.88)
0.118 0.74 (0.22, 2.49)
1.06 (0.29, 3.88)
0.58 (0.13, 2.71)
0.29 (0.09, 0.95) †
0.29 (0.07, 1.15)
0.52 (0.14, 1.92)
0.93 (0.23, 3.70)
0.41 (0.08, 2.10)
0.24 (0.07, 0.82) †
0.24 (0.06, 1.00)
0.3971.14 (0.26, 5.07)
0.69 (0.16, 2.99)
0.3720.72 (0.35, 1.48)
0.77 (0.37, 1.57)
1.16 (0.57, 2.37)
0.041 † 0.47 (0.23, 0.98) †
0.42 (0.19, 0.91) †
* Adjusted model includes sex, age, and H. pylori as covariates.
† χ 2 P value < 0.05.
‡ Wald P value for category OR < 0.05.
ANEMIA IN A RURAL HAITIAN POPULATION
gastric atrophy, resulting in impaired iron absorption. It is
possible that the majority of subjects in our study had high
bacterial load infection, resulting in the observed correlation
between anemia and H. pylori seroreactivity. It is also pos-
sible that we observed an inverse association because of an
unmeasured confounding variable (e.g., socioeconomic status,
location, or inherited disease). Additional investigation of our
Haitian population, including measurements of bacterial load
and iron status indicators, would expand our understanding of
the relationship between anemia and H. pylori infection.
Our study had several limitations that restrict the general-
izability of the results. The population examined was a conve-
nience sample composed of patients likely less healthy than
those people in the general population of the Central Plateau.
The small pediatric sample size may have limited this study’s
power to detect associations in the logistic regression models.
In addition, the rapid H. pylori antibody test used indicated
current or past infection, which could possibly overestimate
the prevalence of infection, thus minimizing the association
between H. pylori and anemia. Some studies indicate that
stool antigen tests are more sensitive and specific for current
H. pylori infection, especially in children. 32 Finally, the number
of subjects recruited was significantly larger than the number
with complete data because of the logistical challenges of data
collection at a mobile clinic ( Figure 1 ). As a result, we cannot
make wider conclusions about the prevalence of anemia in the
Central Plateau of Haiti or the causes of anemia. Nevertheless,
this study is a unique glimpse at an understudied and under-
In developing countries, the impact of anemia may be sig-
nificantly diminished through public health interventions such
as deworming programs, food assistance, iron-fortified com-
plementary foods, 22 iron supplementation, 33, 34 and home food
fortification with micronutrient powders. 14, 35– 39 Given the high
prevalence of anemia and malnutrition in this population, it
is obviously appropriate to study the effects of public health
interventions such as micronutrient fortification powders, 37
AK-1000 (Akamil) fortified home supplement, 40 deworming, 41
and maternal education on infant nutrition. 20
Finally, the devastating January 2010 earthquake and the
subsequent cholera epidemic have likely exacerbated the situ-
ation and increased the prevalence of anemia and malnutri-
tion in this rural Haitian population. Although there have been
many efforts in Haiti surrounding infectious disease and disas-
ter management, these findings highlight the urgent need for
additional study of the etiologies of malnutrition and anemia
in rural populations and targeted public health interventions.
Received February 17, 2011. Accepted for publication July 30, 2011.
Acknowledgments: We are grateful to the students and faculty of
Emory Medishare for assistance in data collection, Sameer Kapadia
for assistance with data entry, two anonymous reviewers for help-
ful comments, and the staff of Project Medishare for their tireless
Financial support: This work was supported in part by National
Institutes of Health Grant T32GM08169 (J.R.S. and R.A.S.). We
thank Quidel Corporation for donating QuickVue Rapid Whole Blood
Antibody Tests for use in this study; Quidel had no role in design of
the study, interpretation of the data, preparation of the manuscript, or
decision to publish.
Authors’ addresses: Joshua R. Shak, Jamie B. Sodikoff, Rebecca A.
Speckman, Francois G. Rollin, and Parminder S. Suchdev, Emory
University School of Medicine, Atlanta, GA, E-mails: jshak@emory
.edu , firstname.lastname@example.org , email@example.com , frollin@gmail
.com, and firstname.lastname@example.org. Marie P. Chery, Project
Medishare for Haiti, Miami, FL, E-mail: email@example.com .
Conrad R. Cole, Cincinnati Children’s Hospital Medical Center,
Cincinnati, OH, E-mail: firstname.lastname@example.org.
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