RESEARCH ARTICLE Open Access
High body mass index is not associated with
atopy in schoolchildren living in rural and urban
areas of Ghana
Irene A Larbi1,2, Kerstin Klipstein-Grobusch1,3*, Abena S Amoah2, Benedicta B Obeng4, Michael D Wilson2,
Maria Yazdanbakhsh4 and Daniel A Boakye2
Abstract
Background: Factors which determine the development of atopy and the observed rural-urban gradient in its
prevalence are not fully understood. High body mass index (BMI) has been associated with asthma and potentially
atopy in industrialized countries. In developing countries, the transition from rural to urban areas has been
associated with lifestyle changes and an increased prevalence of high BMI; however, the effect of high BMI on
atopy remains unknown in this population. We therefore investigated the association between high BMI and atopy
among schoolchildren living in rural and urban areas of Ghana.
Methods: Data on skin prick testing, anthropometric, parasitological, demographic and lifestyle information for
1,482 schoolchildren aged 6-15 years was collected. Atopy was defined as sensitization to at least one tested
allergen whilst the Centres for Disease Control and Prevention (CDC, Atlanta) growth reference charts were used in
defining high BMI as BMI ≥ the 85th percentile. Logistic regression was performed to investigate the association
between high BMI and atopy whilst adjusting for potential confounding factors.
Results: The following prevalences were observed for high BMI [Rural: 16%, Urban: 10.8%, p < 0.001] and atopy
[Rural: 25.1%, Urban: 17.8%, p < 0.001]. High BMI was not associated with atopy; but an inverse association was
observed between underweight and atopy [OR: 0.57, 95% CI: 0.33-0.99]. Significant associations were also observed
with male sex [Rural: OR: 1.49, 95% CI: 1.06-2.08; Urban: OR: 1.90, 95% CI: 1.30-2.79], and in the urban site with older
age [OR: 1.76, 95% CI: 1.00-3.07], family history of asthma [OR: 1.58, 95% CI: 1.01-2.47] and occupational status of
parent [OR: 0.33, 95% CI: 0.12-0.93]; whilst co-infection with intestinal parasites [OR: 2.47, 95% CI: 1.01-6.04] was
associated with atopy in the rural site. After multivariate adjustment, male sex, older age and family history of
asthma remained significant.
Conclusions: In Ghanaian schoolchildren, high BMI was not associated with atopy. Further studies are warranted
to clarify the relationship between body weight and atopy in children subjected to rapid life-style changes
associated with urbanization of their environments.
Background
Allergic diseases are among the most prevalent chronic
conditions in pediatric populations [1]. Although, the
high infectious disease burden in Africa has resulted in
the setting of health priorities around human immuno-
deficiency virus, tuberculosis and malaria; recent studies
indicate that childhood allergies are an emerging health
problem for Africa [2,3]. Moreover, the observed rural-
urban gradient in the prevalence of allergies [2-5] has
raised concerns as to whether the high prevalence in
urban areas is due to environmental changes or if urban
populations are just becoming prone to allergies.
Though there is a paucity of literature on the effect of
migration within non-industrialized countries on aller-
gies, findings of international migrant studies indicate
that migration from developing to industrialized
* Correspondence: kerstin.klipstein-grobusch@wits.ac.za
1Division of Epidemiology & Biostatistics, School of Public Health, Faculty of
Health Sciences, University of the Witwatersrand, Johannesburg, South Africa
Full list of author information is available at the end of the article
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© 2011 Larbi et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons
Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in
any medium, provided the original work is properly cited.
countries is associated with an increased prevalence of
allergies [6].
In view of the fact that the African continent is currently
experiencing a rapid drift in rural-urban migration and the
fact that children under the age of 15 years, who are worst
affected by allergies, constitute about 50 percent of the
population in developing countries, [5] it is crucial to
understand the factors which determine the rural-urban
gradient in the prevalence of allergies. Atopy, the genetic
predisposition of some individuals to develop immunoglo-
bulin E antibodies (IgE) in response to allergen exposure
[7], normally precedes the development of allergies [8] and
accounts for about 50 percent of all cases of allergies
[9-12]. The factors which influence the development of
atopy are however not fully understood [13].
High body mass index (BMI) has been implicated in
the development of asthma in industrialized countries
[14] however, the relationship between high BMI and
atopy is not clearly established [15], but potentially
mediated through elevated production of leptin, tumor
necrosis factor a (TNFa) and interleukin-6 associated
with increased adiposity. High levels of TNFa cause an
increase in the production of T-helper lymphocyte type
2 (Th2) cytokines such as interleukin-4 and interleukin-
5; which are primary signals for activating an immune
response towards atopy [15].
Like in many developing economies in the world,
over-nutrition exist side-by-side with under-nutrition in
the Ghanaian population. Though statistics are not read-
ily available for children of school-going age in Ghana,
records for children under the age of five indicate that
the prevalence of overweight increased by 3.8 folds
(from 0.5% to 1.9%) between 1988 and 1994 [16]. As of
2008, the national prevalence of overweight was 5% in
children under the age of five [17].
Previous studies have reported that the prevalence of
childhood atopy is usually low in rural areas in Africa
where children are normally shorter and lighter than
their urban counterparts [3,18,19] however; the effect of
high BMI, which is increasingly becoming more preva-
lent in developing countries [20,21] on atopy has barely
been explored in rural and urban areas in Africa. The
current study sought to explore the effect of high BMI
on atopy among school children living in rural and
urban areas of Ghana.
Methods
Study sites
This study was conducted in 2006 in three districts in
the Greater Accra Region of Ghana; two urban (Accra
Metropolitan Area and Ga) and one rural district
(Dangme East) (see Figure 1). Compared to rural settle-
ments, urban areas are more developed in terms of
basic infrastructure and lifestyle.
Study population
The study population comprised children attending
mixed day basic-level schools in the three selected dis-
tricts who were in the age range of 6-15 years. The
recruited schools in the rural site were public whilst
those in the urban site were mainly public and middle-
class private schools. The response rate for the study
was 59% [urban site: 54% (1111/2064); rural site: 68%
(815/1200)]. Parents or guardians consented to their
children’s participation in the study by signing or thumb
printing a consent form. Ethical approval for the study
was granted by the Institutional Review Board of the
Noguchi Memorial Institute for Medical Research in
Accra and the Human Research Ethics Committee of
the University of the Witwatersrand, Johannesburg.
Measurements
Atopy
Atopy was assessed by skin prick testing (SPT) on the
volar forearms of each participant with a panel of stan-
dardized allergen extracts [house dust mite (Dermato-
phagoides sp), cockroach (Blattella germenica) and
peanut (Arachis hypogaea)] from ALK-Abello, Denmark;
and some selected fresh fruits (pineapple, mango,
banana, papaya, orange, and apple) which are widely
consumed in Ghana. The prick-prick procedure, which
involves dipping the tip of the skin lancet into a cut
portion of the fresh fruit and then pricking the skin
with the fruit residue, was used in testing the fruits. His-
tamine and diluent (ALK-Abello, Denmark) respectively,
were used as positive and negative controls. The cut-off
for defining a positive reaction to an allergen was an
average wheal size of 3 mm (or more) greater than the
wheal produced by diluent; and histamine positivity (i.e.
wheal size ≥ 3 mm). The results were read 15 minutes
after pricking.
Anthropometry
Height and weight were measured using a portable free-
standing stadiometer and an electronic scale (BS-8001,
capacity: 130 kg) respectively. Participants were mea-
sured wearing school uniforms and no shoes. In measur-
ing weight, each participant was made to stand still in
an upright position on the scale. Weight was recorded
to the nearest 0.1 kg whilst height was recorded to the
nearest 0.5 cm.
Parasitological survey
Participants were asked to provide fresh stool samples
in the morning and to submit urine samples between
11:00 and 13:00 hours when maximum shedding of
schistosome eggs is known to occur in humans. The
Kato-Katz [22] and urine filtration [23] techniques
were respectively used in processing stool and urine
samples to determine the presence of intestinal hel-
minths and urinary schistosomes. The intensity of
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infection for intestinal helminths was expressed as
number of eggs per gram of faeces whilst the intensity
of urinary schistosomes was expressed as number of
eggs per 10 ml of urine.
Questionnaire survey
Information on potential confounding factors such as;
breast-feeding duration, highest educational level and
occupation of the person who provided financially for
the child (used as proxy measures for socio-economic
status), family history of asthma (measured as physician-
diagnosed asthma in parents, siblings, grandparents or
parents’ siblings), source of domestic fuel (i.e. fuel used
for cooking at home) and exposure to passive cigarette
smoke was obtained through a standardized interviewer-
administered questionnaire survey which targeted par-
ents/guardians of the children. The interviews were con-
ducted in the homes of the study participants in English
and local Ghanaian languages such as Akan and Ga-
Adangme in some cases. Information on participants’
date of birth was mainly obtained from their antenatal
record cards. Field personnel in this study were trained
to conduct measurements and collect data in a standar-
dized way using objective measures.
Data analysis
Atopy was defined at two levels; atopic (sensitization to
at least one tested allergen) and non-atopic (not sensi-
tized to any tested allergen). BMI was calculated as
weight (kg) divided by the square of height (m). NutStat,
a programme in Epi-Info version 3.3.2 (CDC, Atlanta,
Ga., USA), was used in computing the standardized
BMI percentiles for age and sex. Based on the CDC
growth charts [24], high BMI was defined at the follow-
ing levels; normal weight: BMI ≥ 5th percentile and <
85th percentile, underweight: BMI < 5th percentile, over-
weight: BMI ≥ 85th percentile and < 95th percentile and
obese: BMI ≥ 95th percentile. For the purpose of this
analysis, categories for overweight and obese were
merged and referred to as high BMI. Confounding vari-
ables were categorized into 3-5 closed-ended levels. To
allow all observations to be used in estimating the effect
of non-missing observations in the analysis, dummy
values were generated for the missing observations of
each variable. This was done by creating a missing cate-
gory for the missing values of each variable. Analysis of
variance was used in testing the differences in the mean
of height, weight and BMI in the rural and urban sites,
Figure 1 Map of the Greater Accra Region showing locations of the recruited rural and urban schools.
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whilst adjusting for the effect of age. Logistic regression
was used in investigating the association of high BMI
and atopy, taking into account confounding factors. A
variable was retained in the multivariate model if the p-
value corresponding to the unadjusted odds ratio was ≤
0.10. Sex differentials in urban, respectively rural partici-
pants were assessed by inclusion of interaction terms; a
p-value of ≤ 0.05 for an interaction term was regarded
as evidence of interaction. All analyses were performed
using Stata version 9.2 (Stata Corp., College Station,
TX).
Results
Baseline characteristics
The baseline characteristics of the study population are
presented in Table 1. The mean age for the 1482 school
children was 10.51 (± 2.29) years and was significantly
higher for urban [11.07, (95% CI: 10.90-11.25)] than
rural [9.95, (95% CI: 9.80-10.09)] participants. After
adjusting for age, the mean height (cm) [urban: 141.96,
(95% CI: 141.01-142.90); rural: 131.66, (95% CI: 130.90-
132.41)] and weight (kg) [urban: 35.61, (95% CI: 34.80-
36.42); rural: 31.03, (95% CI: 30.50-31.56)] differed sig-
nificantly by residence with participants in the urban
site being generally taller and heavier.
Prevalence of high BMI
The prevalence of high BMI, based on standardized
BMI-for-age and sex, was 16% (118/740) in the rural
site and 10.8% (80/742) in the urban site (p < 0.001).
The overall prevalence of high BMI in the study popula-
tion was 13.4% (198/1482): 13.5% (105/776) in females
[urban site: 13.4% (53/395); rural site: 13.6% (52/381)]
and 13.2% (93/706) in males [urban site: 7.8% (27/347);
rural site: 18.4% (66/359)] (see Figure 2).
Prevalence of sensitization to individual allergens
Overall, 13.6% [rural: 101/740, urban: 101/742] of the
study participants were sensitized to dust mite, 10.8%
[rural: 104/740, urban: 56/742, p = 0.000] to cockroach
and 1.9% [rural: 15/740, urban: 13/742, p = 0.697] to
peanut. The prevalence of sensitization to any of the
tested fruits was 3.8% [rural: 24/740, urban: 33/742, p =
0.228]; and of these, pineapple was found to be the
most allergenic [1.82% (27/1482)].
Prevalence of atopy
25.1% [186/740] of the rural participants and 17.8%
[132/742] of the urban participants were found to be
atopic; with the overall prevalence of atopy being 21.5%
(318/1,482). A higher prevalence of atopy was observed
in males [rural: 29.0% (104/359); urban: 22.8% (79/347)]
than females [rural: 21.5% (82/381); urban: 13.4% (53/
Table 1 Baseline characteristics of 1,482 school children
aged 6-15 years in urban and rural areas of the Greater
Accra Region of Ghana
Variable Urban
(%)
Rural
(%)
Total p-value**
All 742 740 1,482
Sex
Males 347
(46.77)
359
(48.51)
706 (47.64) 0.501
Females 395
(53.23)
381
(51.49)
776 (52.36)
Age
6-8 years 133
(17.92)
191
(25.81)
324 (21.86) 0.000
9-11 years 261
(35.18)
347
(46.89)
608 (41.03)
12-15 years 348
(46.90)
202
(27.30)
550 (37.11)
Nutritional status indicators
Normal weight 568
(76.55)
599
(80.95)
1,167 (78.74)
0.000
Underweight 94 (12.67) 23 (3.11) 117 (7.89)
High BMI 80 (10.78) 118
(15.95)
198 (13.36)
Atopy
Non-atopic 610
(82.21)
554
(74.86)
1164 (78.54)
0.001
Atopic 132
(17.79)
186
(25.14)
318 (21.46)
S. haematobium infection
Not infected 714
(97.28)
630
(90.00)
1,344 (93.72)
0.000
Infected 20 (2.72) 70 (10.00) 90 (6.28)
Intestinal parasites infection
Not infected 659
(97.34)
434
(57.81)
1, 093 (82.99)
0.000
Hookworm 13 (1.92) 76 (11.88) 89 (6.76)
Trichuris sp 2 (0.30) 16 (2.50) 18 (1.37)
Ascaris sp 0 (0.00) 93 (14.53) 93 (7.06)
ЖCo-infected 3 (0.44) 21 (3.28) 24 (1.82)
Passive smoking
Non-exposed 398
(66.22)
218
(69.43)
616 (67.32) 0.327
Exposed 203
(33.78)
96 (30.57) 299 (32.68)
Source of domestic fuel
Liquefied Petroleum Gas (LPG) 368
(61.13)
5 (1.59) 373 (40.68) 0.000
Charcoal 184
(30.56)
111
(35.24)
295 (32.17)
Firewood 50 (8.31) 199
(63.17)
249 (27.15)
Family history of asthma
No 352
(59.26)
174
(55.24)
526 (57.87) 0.338
Yes 170
(28.62)
105
(33.33)
275 (30.25)
No idea 72 (12.12) 36 (11.43) 108 (11.88)
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395)]. The prevalence of atopy in the study population
also increased considerably with age [6-8 years: 18.8%
(61/324); 9-11 years: 20.7% (126/608); 12-15 years:
23.8% (131/550)]; however, this increase was more pro-
found in the urban site (data not shown).
Association between high BMI and atopy
Details of the relationship between the study parameters
and atopy are given in Table 2. Using normal weight as
our reference, high BMI and atopy were not associated
in the study population; whereas underweight was found
to be inversely associated with atopy after multivariate
adjustment [OR: 0.57, 95% CI: 0.33-0.99; p = 0.045].
However, this effect was only significant in males [OR:
0.49, 95% CI: 0.25-0.98; p = 0.045].
Association of other study parameters with atopy
In both the rural [OR: 1.49, 95% CI: 1.06-2.08] and
urban [OR: 1.90, 95% CI: 1.30-2.79] sites, males had an
increased likelihood of being atopic compared to
females. The likelihood of atopy was also increased in
older urban children [OR: 1.76, 95% CI: 1.00-3.07] and
those with a family history of asthma [OR: 1.57, 95% CI:
1.10-2.23]. No regular trend was observed across the
various levels of parent’s occupation and atopy. How-
ever, on recoding parent’s occupation into a binary vari-
able (unemployed and employed), the likelihood of
atopy was observed to be decreased [OR: 0.33, 95% CI:
0.12-0.93] in urban participants with employed parent
(s). Being co-infected with two or more intestinal para-
sites in the rural site was associated with increased odds
of atopy by more than two-folds [OR: 2.47, 95% CI:
1.01-6.04].
Stratification by sex for rural and urban participants
showed decreased likelihood of atopy for urban females
with employed parents (OR: 0.22, 95% CI: 0.05-0.99)
and increased likelihood of atopy for urban males aged
12-15 years (OR: 2.18, 95% CI: 1.02-4.66). Rural females
were significantly more likely to be atopic if intestinal
parasite co-infection occurred (OR:4.69; 95% CI 1.30-
16.93) and if their parents attended school for 7-9 years
(OR: 2.68, 95% CI: 1.17-6.15) or had tertiary education
(OR: 4.89, 95% CI 1.73-13.80). Inclusion of a sex/educa-
tional attainment interaction term in the logistic regres-
sion model showed significant interaction (p = 0.003),
whereas interaction terms for sex and age, parent’s edu-
cational attainment or intestinal parasite co-infection
were not significant.
After multivariate adjustment, the following variables
remained significantly associated with atopy: male sex
[rural: OR: 1.45, 95% CI: 1.03-2.04; urban: OR: 2.10, 95%
CI: 1.41-3.13], family history of asthma [OR: 1.56, 95%
CI: 1.09-2.24] and older age (i.e. 12-15 years) in the
urban site [OR: 1.89, 95% CI: 1.05-3.42].
Discussion
High BMI in this population of Ghanaian school chil-
dren aged 6 to 15 years was not associated with atopy
in both the rural and urban sites. However, underweight
children were found to have a reduced likelihood of
atopy. Other factors such as sex, older age, family his-
tory of asthma, occupational status of parents, educa-
tional level of parents and co-infection with intestinal
parasites were associated with atopy in univariate analy-
sis; whilst male sex, older age, and family history of
asthma remained the significant predictors of atopy after
multivariate adjustment. In the rural site a higher preva-
lence of high BMI and atopy were observed than in the
urban site in this study.
In line with previous studies, the urban participants in
our study were considerably taller and heavier than their
rural counterparts [3,18]. Compared to studies in other
parts of Ghana [3], the anthropometric parameters for
this study population are slightly lower; but this could
be attributed to the lower mean age of our study
population.
Previous studies have often shown a link between
lower levels of physical activity and high BMI [21].
However, children in most rural settings in Africa are
normally expected to participate in the household
chores which may include working on the farm, carrying
Table 1 Baseline characteristics of 1,482 school children
aged 6-15 years in urban and rural areas of the Greater
Accra Region of Ghana (Continued)
Exclusive breast feeding
None 74 (18.23) 48 (10.39) 122 (14.06.) 0.002
1-6 months 280
(68.97)
360
(77.92)
640 (73.73)
6-12 months 52 (12.81) 54 (11.69) 106 (12.21)
Educational level of parent
No formal education 124
(27.43)
148
(30.14)
272 (28.84) 0.011
7-9 years education 178
(39.38)
165
(33.60)
343 (36.37)
10-15 years education 68 (15.04) 108
(22.00)
176 (18.66)
Tertiary education 82 (18.14) 70 (14.26) 152 (16.12)
Occupation of parent
Unemployed 16 (3.56) 14 (2.86) 30 (3.20) 0.542
Trader 76 (16.93) 139
(28.43)
215 (22.92)
Farmer 95 (21.16) 83 (16.97) 178 (18.98)
Public servant 168
(37.42)
169
(34.56)
337 (35.93)
Business 94 (20.94) 84 (17.18) 178 (18.98)
Ж Co-infection: infected with two or more intestinal helminthes
** Comparison between urban and rural areas. Totals may differ due to
missing values of some variables.
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water from the riverside or public taps; and in coastal
communities such as the rural site in this study, accom-
pany their fathers on fishing expeditions (which involves
the paddling of manual canoes). Despite this, a higher
prevalence of high BMI was recorded in our rural
participants in this study. A possible explanation for this
observation could be that early life factors such as mal-
nutrition had increased the risk of central adiposity in
the rural participants. Available records show that the
prevalence of underweight has consistently been high


Figure 2 Distribution of age-standardized BMI by sex in school children aged 6-15 years in the Greater Accra Region of Ghana.
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Table 2 Factors associated with atopy in 1,482 school children aged 6-15 years living in urban and rural areas in the
Greater Accra Region of Ghana
UNIVARIATE ANALYSIS MULTIVARIATE ANALYSIS**
Variable Atopy (%)* Combined
OR (95% CI)
Urban
OR (95% CI)
Rural
OR (95% CI)
Combined
OR (95% CI)
Urban
OR (95% CI)
Rural
OR (95% CI)
Sex
Female 135 (17.4) 1 1 1 1 1 1
Male 183 (25.9) 1.66 (1.29-2.13) 1.90 (1.30-2.79) 1.49 (1.06-2.08) 1.63 (1.26-2.11) 2.10 (1.41-3.13) 1.45 (1.03-2.04)
Age
6-8 years 61 (18.8) 1 1 1 1 1 1
9-11 years 126 (20.7) 1.13 (0.80-1.58) 1.12 (0.61-2.05) 1.15 (0.76-1.75) 1.14 (0.80-1.63) 1.19 (0.63-2.24) 1.18 (0.76-1.82)
12-15 years 131 (23.8) 1.35 (0.96-1.90) 1.76 (1.00-3.07) 1.32 (0.83-2.09) 1.36 (0.95-1.96) 1.89 (1.05-3.42) 1.28 (0.79-2.07)
Nutritional status indicators
Normal weight 254 (21.8) 1 1 1 1 1 1
Underweight 254 (21.8) 0.61 (0.36-1.04) 0.58 (0.30-1.12) 1.08 (0.42-2.78) 0.57 (0.33-0.99) 0.52 (0.26-1.02) 1.07 (0.40-2.83)
High BMI 47 (23.7) 254 (21.8) 1.12 (0.78-1.60) 1.00 (0.55-1.83) 1.13 (0.73-1.77) 1.17 (0.81-1.69) 1.23 (0.66-2.29) 1.17 (0.73-1.87)
Passive smoking
Non-exposed 125 (20.3) 1 1 1
Exposed 61 (20.4) 1.00 (0.71-1.42) 0.78 (0.50-1.23) 1.54 (0.89-2.66)
Family history of asthma
No 94 (17.9) 61 (20.4) 1 1 1 1 1 1
Yes 70 (25.5) 1.57 (1.10-2.23) 1.58 (1.01-2.47) 1.52 (0.86-2.67) 1.56 (1.09-2.24) 1.54 (0.97-2.46) 1.41 (0.79-2.53)
No idea 20 (18.5) 1.04 (0.61-1.78) 0.80 (0.39-1.65) 1.53 (0.67-3.46) 0.99 (0.58-1.72) 0.68 (0.32-1.43) 1.56 (0.68-3.60)
Occupational status of parent
Unemployed 9 (30.0) 1 1 1 1 1 1
Employed 183 (20.2) 0.59 (0.27-1.31) 0.33 (0.12-0.93) 1.13 (0.31-4.13) 0.65 (0.29-1.47) 0.33 (0.11-1.00) 1.26 (0.32-4.95)
Source of domestic fuel
LPG*** 77 (20.6) 1 1 1
Charcoal 50 (16.9) 0.78 (0.53-1.16) 0.75 (0.47-1.19) 0.88 (0.09-8.29)
Firewood 59 (23.7) 1.19 (0.81-1.75) 0.52 (0.22-1.28) 1.45 (0.16-13.29)
Exclusive breast feeding
None 22 (18.0) 1 1 1
1-6 months 138 (21.6) 1.25 (0.76-2.06) 1.29 (0.62-2.70) 1.01 (0.51-2.03)
6-12 months 17 (16.0) 0.87 (0.43-1.74) 1.34 (0.50-3.57) 0.52 (0.19-1.41)
Educational level of parent
No formal education 57 (21.0) 1 1 1 1 1 1
7-9 years education 67 (19.3) 0.92 (0.62-1.36) 0.76 (0.43-1.37) 1.09 (0.64-1.87) 0.92 (0.61-1.39) 0.68 (0.37-1.26) 0.97 (0.56-1.70)
10-15 years education 35 (19.9) 0.94 (0.58-1.50) 0.43 (0.18-1.06) 1.32 (0.74-2.37) 0.98 (0.60-1.59) 0.44 (0.17-1.10) 1.24 (0.68-2.26)
Tertiary education 34 (22.4) 1.09 (0.67-1.76) 0.78 (0.38-1.59) 1.51 (0.79-2.90) 1.07 (0.65-1.75) 0.67 (0.32-1.41) 1.36 (0.70-2.65)
Intestinal parasite infection
Not infected 218 (20.0) 1 1 1 1 1
Hookworm 26 (29.2) 1.66 (1.02-2.68) 1.39 (0.38-5.13) 1.43 (0.84-2.45) 1.39 (0.84-2.83) - 1.34 (0.77-2.33)
Trichuris sp 5 (27.8) 1.54 (0.54-4.28) - 1.50 (0.51-4.41) 1.53 (0.53-4.39) - 1.50 (0.50-4.50)
Ascaris sp 19 (20.4) 1.03 (0.61-1.74) - 0.85 (0.49-1.47) 1.00 (0.57-1.74) - 0.79 (0.45-1.38)
Co-infected 9 (37.5) 2.41 (1.04-5.58) - 2.47 (1.01-6.04) 2.13 (0.90-5.04) - 2.23 (0.90-5.58)
S. haematobium infection
No 290 (21.6) 1 1 1
Yes 20 (22.2) 1.04 (0.62-1.74) 0.81 (0.23-2.80) 0.93 (0.52-1.65)
* Totals for atopy may differ due to missing values of some variables.
** Adjusted for all other variables in the analysis. For inclusion in the multivariate model, a variable’s p-value for the unadjusted odds ratio had to be ≤ 0.10
*** LPG: Liquefied Petroleum Gas
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among children under the age of five in rural areas in
Ghana [17]. Studies have shown that malnutrition
occurring in early life compromises linear growth, with
subsequent availability of food potentially increasing the
risk of central adiposity due to the increase in body
weight but not height [25].
Previous studies in Ghana [26] and other parts of
Africa [4] have generally reported a higher prevalence of
sensitization to dust mite and cockroach allergens as
compared to allergens from grass pollen and domestic
animals such as cat and dog. The other allergens which
were included in our panel (peanut and fruits), were
used to study the levels of sensitization to these food
items which constitute the diet of many Ghanaians.
Hence, we are convinced that our panel of allergens was
able to detect the majority of atopic children in the
study population. In contrast to previous studies
[3,13,18,27] the current study found a higher prevalence
of atopy in the rural site. A possible explanation for this
observation could be the significantly higher levels of
cockroach sensitivity which was recorded in the rural
site in this study.
The exposure and sensitivity to cockroach allergens
within countries has been shown to exhibit a geographi-
cal variation [28] and the prevalence of cockroach sensi-
tivity has generally been reported to be high among low
socio-economic populations in urban areas [29]. Like
most previous studies [30], diagnosis of cockroach sensi-
tivity in this study was based on sensitization to Blat-
tella germenica. However, other species of cockroaches
such as Periplaneta americana and Blatta orientalis are
common in Ghana; though there are no available data
on their distribution and abundance. Since sensitization
to cockroach allergen is dependent on exposure and
most cockroach allergens have been reported to be spe-
cies-specific [28], it is likely that Blattella germenica is
more prevalent in the rural than the urban site in this
study. Further studies are however required to investi-
gate this.
The association between high BMI and atopy has been
explored in cross-sectional [13,30-32], case control
[19,33] and cohort [34] studies with often inconsistent
findings. Positive associations have been reported in
cross-sectional surveys on Taiwanese teenagers [13]
Caucasian Australian children [32] and American chil-
dren [31], whereas a study in Chinese school children
did not find an association between obesity and atopy
[35]. In this study, high BMI was not associated with
atopy, whereas a significant inverse association was
observed between underweight and atopy in males. This
supports studies which have reported that skin test sen-
sitivity is low in thin children [19] but contradicts the
findings of a similar survey in Belgium [31] where
underweight girls were found to have an increased risk
of atopy. Our finding could partly be explained by pre-
vious studies in animal models [36] which showed that
the production of primary signals for atopy such as
interleukin-4 is down-regulated when nutritional intake
is reduced. This is mainly because levels of circulating
leptin, interleukin-6, interleukin-8, C-reactive protein,
plasminogen activator inhibitor-1 and haptoglobin,
which are all markers of inflammation, are considerably
decreased in underweight individuals [15] High levels of
these markers collectively contribute to the skewing of
the immune system towards a T-helper lymphocyte type
2 (Th2) cytokine profile which results in an increased
risk of atopy [15]. Hence, it is possible that reduced
levels of these markers may increase immune tolerance
to antigens in underweight individuals. Reasons why this
inverse association was only observed in males are not
immediately known but could be due to the higher pro-
portion of underweight males than females (57.3% vs.
42.7%) in this study. Previous studies have reported
positive associations between underweight and asthma
in boys [37,38]. However, these studies did not verify if
reported asthma was due to atopic or non atopic
mechanisms. In this study, no information was collected
on asthma symptoms, thus not allowing us to comment
on implications with regard to asthma development.
The higher prevalence of atopy which was observed
among males in this study is in line with the findings of
other studies [13]. Family history of asthma has been
shown to increase susceptibility to atopy whilst the risk
of atopy increases with the age of children [39]. As
exposure normally precedes sensitization, it is possible
that the degree of allergen exposure increases with age.
Hence, the more profound increase in atopy with age in
the urban site could be attributed to the higher mean
age of the urban participants in this study.
Over the years, most studies [3] have consistently
shown a link between higher socio-economic status
(SES) and atopy. Some of the plausible explanations
which have been offered for this association include bet-
ter nutritional status at higher SES in turn influencing
the function of T-lymphocyte cells. SES may influence
the production of IgE through T-helper lymphocyte cell
function [39]. In this study, the employment status and
educational levels of parents were used as proxy mea-
sures of SES and the observed association between par-
ental educational level and atopy is consistent with
some previous studies [13]. This notwithstanding, rea-
sons for the observed inverse association with parent’s
employment status are quite unclear but could be due
to confounding by factors such as diet which was not
measured in this study.
Early studies on allergy among helminth infected
populations in parts of Africa often reported that the
levels of allergic sensitization in such populations were
Larbi et al. BMC Public Health 2011, 11:469
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low compared to non-infected populations. Hence, it
was suggested that Th2-inducing infections might actu-
ally protect against atopy [5,6]. More recent studies have
shown that the role of helminth infections in the devel-
opment of allergy may not always be protective but
could be influenced by the intensity or chronicity of
infections [6]. For instance, children with wealthy par-
ents often tend to exhibit higher levels of atopy and har-
bour lower helminth burdens whilst the converse applies
to children with poor parents. Therefore, it has been
proposed that SES may influence the burden of hel-
minth infections through nutritional status which conse-
quently influences T-helper lymphocyte cell function
[40]. Hence, light acute infections may enhance atopy
whilst heavy and chronic infections may inhibit it [6,41].
In this study, we found that infection with two or more
intestinal helminths at the same time in an individual
was associated with an increased likelihood of atopy in
the rural site. It is possible that the combined effect pro-
duced by different species of intestinal helminths when
they occur together might be different from when they
occur individually.
With the rapid increase in rural-urban migration in
sub-Saharan African countries and the rise in childhood
allergy cases in urban areas, it was important to deter-
mine if high body weight which is increasingly becoming
common in developing countries influences the develop-
ment of atopy. To our knowledge, this is the first study
which has examined the relation between high BMI on
atopy in rural and urban settings in West Africa. Field
personnel in this study were trained to collect data in a
standardized way using objective measures; hence, the
potential for misclassification of atopy and BMI was
kept to a minimum. Though there were missing obser-
vations of some variables, our analyses showed that the
missing observations did not significantly influence the
findings of the study. Regardless of this, the results of
this study should be interpreted in the context of a
response rate of 59% and the potential for selection bias.
Whereas parents from lower socio-economic levels may
regard research as an easier means of getting free access
to health care, the converse applies to parents in higher
socio-economic levels. Hence, our study population in
the urban site consists mainly of participants from pub-
lic and middle-high private schools but not the very
high class schools. It is therefore possible that the
observed prevalence of high BMI and atopy in the
urban site does not reflect the true prevalence of these
conditions and that the associations observed between
these two might be biased.
The use of the CDC growth reference charts in classi-
fying nutritional status in this study is another potential
source of bias. Aside from limitations it shares with
other available growth reference charts [42], the CDC
charts had American children as its reference population
[43]. Hence, its application to children in an African
country may not provide accurate estimates.
Conclusion
In our study population of Ghanaian school children,
high BMI was not associated with atopy, whereas sex,
older age and family history of asthma were. These find-
ings do not support obesity as an important risk factor
for atopy status in this population.
List of abbreviations used
BMI: Body Mass Index; 95% CI: 95% Confidence Interval; IgE: immunoglobulin
E antibodies; OR: Odds Ratio; SES: Socio-economic status; SPT: Skin Prick
Testing.
Acknowledgements
The authors wish to acknowledge the director of the Noguchi Memorial
Institute for Medical Research, the study participants, teachers’ in the
participating schools, the National Service Personnel who were attached to
the project and the staff of the Global View of Food Allergy Study in Ghana.
We are also grateful to Dr. Anita Ghansah and Dziedzom deSouza for critical
review of the manuscript. The manuscript is based on a research report for
the degree of Master of Science in Medicine (Epidemiology & Biostatistics),
University of the Witwatersrand, Johannesburg, South Africa.
Financial support for this study was provided by UNICEF/UNDP/World Bank/
WHO Special Programme for Research and Training in Tropical Diseases
(TDR) under a fellowship to IAL. The study was conducted as part of a
European Union funded project (FOOD-CT-2005-517812).
Author details
1Division of Epidemiology & Biostatistics, School of Public Health, Faculty of
Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
2Department of Parasitology, Noguchi Memorial Institute for Medical
Research, University of Ghana, Legon-Accra, Ghana. 3Julius Center for Health
Sciences and Primary Care, Utrecht University Medical Center, Utrecht, The
Netherlands. 4Department of Parasitology, Leiden University Medical Centre,
Leiden, The Netherlands.
Authors’ contributions
IAL designed the study, was involved in data collection and management,
conducted the statistical data analysis and drafted the manuscript. KKG was
involved in the design of the study, guided statistical analysis and
manuscript writing. ASA was involved in data collection and management
and reviewed the manuscript. BOB and MDW were involved in project
implementation and review of the manuscript. MY was responsible for the
overall project coordination of the European Union funded project of which
this study formed a part and reviewed the manuscript. DAB was involved in
the design of the study, the overall project implementation and co-
ordination and reviewed the manuscript. All authors have read and
approved the final manuscript.
Competing interests
The authors declare that they have no competing interests.
Received: 2 December 2010 Accepted: 14 June 2011
Published: 14 June 2011
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Cite this article as: Larbi et al.: High body mass index is not associated
with atopy in schoolchildren living in rural and urban areas of Ghana.
BMC Public Health 2011 11:469.
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