Factors Associated with High Prevalence of Intestinal Protozoan Infections among Patients in Sana'a City, Yemen

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DOI: 10.1371/journal.pone.0022044 · Source: PubMed
Abstract
Intestinal protozoan diseases in Yemen are a significant health problem with prevalence ranging from 18% to 27%. The present study is a cross-sectional study aimed at determining the factors associated with the high prevalence of intestinal protozoan infections among patients seeking health care in Sana'a City, the capital of Yemen. Stool samples were collected from 503 patients aged between 1 and 80 years old; 219 were males and 284 females. Biodata were collected via pretested standard questionnaire. Faecal samples were processed and examined for (oo)cysts or ova using a wet mount preparation after formal-ether concentration technique. Cryptosporidium oocysts were detected using the Ziehl-Neelsen staining technique. The overall prevalence of intestinal protozoan infections was 30.9%. Infection rates of Giardia duodenalis, Entamoeba histolytica/dispar and Cryptosporidium were 17.7%, 17.1% and 1%, respectively. Other parasites detected included Ascaris lumbricoides (2.4%), Schistosoma mansoni (0.3%), Hymenolepis nana (1.4%) and Enterobius vermicularis (0.4%). Multivariate analysis using forward stepwise logistic regression based on intestinal protozoan infections showed that contact with animals (OR = 1.748, 95% CI = 1.168-2.617) and taking bath less than twice a week (OR = 1.820, 95% CI = 1.192-2.779) were significant risk factors of protozoan infections. This present study indicated that intestinal protozoan infections are still a public health problem in Yemen, with Giardia and Entamoeba infections being most common. Statistical analysis indicated that low personal hygiene and contact with animals were important predictors for intestinal protozoan infections. As highlighted in this study, in order to effectively reduce these infections, a multi-sectoral effort is needed. Preventive measures should include good hygienic practices, good animal husbandry practices, heightened provision of educational health programs, health services in all governorates including rural areas. Furthermore, it is also essential to find radical solutions to the recent water crises in Yemen.
Factors Associated with High Prevalence of Intestinal
Protozoan Infections among Patients in Sana’a City,
Yemen
Naelah A. Alyousefi
1
*, Mohammed A. K. Mahdy
1,2
, Rohela Mahmud
1
, Yvonne A. L. Lim
1
*
1 Department of Parasitology, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia, 2 Department of Parasitology, Faculty of Medicine, Sana’a University,
Sana’a, Yemen
Abstract
Background:
Intestinal protozoan diseases in Yemen are a significant health problem with prevalence ranging from 18% to
27%. The present study is a cross-sectional study aimed at determining the factors associated with the high prevalence of
intestinal protozoan infections among patients seeking health care in Sana’a City, the capital of Yemen.
Methodology/Principal Findings:
Stool samples were collected from 503 patients aged between 1 and 80 years old; 219
were males and 284 females. Biodata were collected via pretested standard questionnaire. Faecal samples were processed
and examined for (oo)cysts or ova using a wet mount preparation after formal-ether concentration technique.
Cryptosporidium oocysts were detected using the Ziehl-Neelsen staining technique. The overall prevalence of intestinal
protozoan infections was 30.9%. Infection rates of Giardia duodenalis, Entamoeba histolytica/dispar and Cryptosporidium
were 17.7%, 17.1% and 1%, respectively. Other parasites detected included Ascaris lumbricoides (2.4%), Schistosoma mansoni
(0.3%), Hymenolepis nana (1.4%) and Enterobius vermicularis (0.4%). Multivariate analysis using forward stepwise logistic
regression based on intestinal protozoan infections showed that contact with animals (OR = 1.748, 95% CI = 1.168–2.617)
and taking bath less than twice a week (OR = 1.820, 95% CI = 1.192–2.779) were significant risk factors of protozoan
infections.
Conclusions/Significance:
This present study indicated that intestinal protozoan infections are still a public health problem
in Yemen, with Giardia and Entamoeba infections being most common. Statistical analysis indicated that low personal
hygiene and contact with animals were important predictors for intestinal protozoan infections. As highlighted in this study,
in order to effectively reduce these infections, a multi-sectoral effort is needed. Preventive measures should include good
hygienic practices, good animal husbandry practices, heightened provision of educational health programs, health services
in all governorates including rural areas. Furthermore, it is also essential to find radical solutions to the recent water crises in
Yemen.
Citation: Alyousefi NA, Mahdy MAK, Mahmud R, Lim YAL (2011) Factors Associated with High Prevalence of Intestinal Protozoan Infections among Patients in
Sana’a City, Yemen. PLoS ONE 6(7): e22044. doi:10.1371/journal.pone.0022044
Editor: Christopher N. Mores, Louisiana State University, United States of America
Received March 9, 2011; Accepted June 14, 2011; Published July 18, 2011
Copyright: ß 2011 Alyousefi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by research grants from the University of Malaya (Grant no. PS204/2010A, RG181/10HTM and RG221/10HTM). The funders
had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have decl ared that no competing interests exist.
* E-mail: naelaalyousfi@yahoo.com (NAA); limailian@um.edu.my (YALL)
Introduction
Yemen is a developing Middle Eastern country located at the
southern part of the Arabian Peninsula with a total population of
23 million (Figure 1). The country depends totally on ground
water and rain water as a source of water. Recently, the country
has fallen into a deep water crisis characterized by very rapid
mining of groundwater, extreme water supply shortages in the
major cities, and limited access of the population to safe drinking
water. WHO reported that only 25% of the population had easy
access to safe water [1]. Being one of the poorest countries in the
Middle East with a per capita income of approximately USD510,
42% of Yemen’s total population is estimated to be under the
national poverty line [2]. The poverty ratio is higher in the rural
area where 75% of population lives and only 25% is covered with
health care services compared to 80% of urban area. This
economic imbalance coupled with the current water scarcity have
also encouraged or sustained the high prevalence of intestinal
protozoan infections in Yemen.
Although intestinal parasitic infections had received attention in
Yemen as early as 1950s, most of these efforts were to combat
schistosomiasis, unfortunately neglecting the other intestinal
parasites [3,4]. In 1985, a large scale survey by Raja between
1982–1983 involving 37,000 stool specimens showed that 53% of
the study population had intestinal parasitic infections with
Trichuris trichiura, Ascaris lumbricoides and Giardia duodenalis recording
high prevalences [5]. In 2000, Raja and his colleagues carried out
another survey in seven villages in the rural areas of Ibb
governorate. In this study, the prevalence of G. duodenalis and
Entameoba histolytica/dispar was 18% and 14%, respectively [6]. A
recent study carried out on 303 restaurant workers in 58
restaurants in Sana’a City reported high prevalence of G. duodenalis
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(35.3%) and E. histolytica/dispar (48.9%) [7]. The infection rates of
G. duodenalis and E. histolytica/dispar were also reported at 18.2%
and 52%, respectively, in a similar study conducted on 132
restaurant workers in Almukala City, Hadramowat [8]. The high
prevalence of these two intestinal protozoa among restaurant
workers is alarming with the possible risk of foodborne outbreak.
Hitherto several studies have focused on parasitic infections
among children in Yemen. A cross-sectional study, carried out on
104 children from lowland and highland areas in the south of
Yemen showed that, the prevalence of G. duodenalis in the lowland
and highland areas were 34.6% and 35.1%, respectively. Children
living in the lowland areas had higher infection rate of E.
histolytica/dispar (42.3%) compared to those living in the highland
areas (36.8%) [9]. In a hospitalized based study carried out on
9,014 children in the pediatric health center in Sana’a City, the
prevalence of G. duodenalis and E. histolytica/dispar was 16.7% and
11.7%, respectively [10]. A recent study among children in
orphanages, reported high prevalence of G. duodenalis (26.8%), E.
histolytica/dispar (13%) and Cryptosporidium (24%) [11]. Another
study on children was in Hadramowat in 2010 which recorded
prevalence of 19.2% for Giardia and 16.8% for E. histolytica/dispar
infections, highlighting that parasitosis reflected the prevalent
hygienic problems and their influences on public health of
Hadramowat [12].
What was alarming in Yemen was that most studies in different
localities and different populations have shown a high prevalence
of intestinal protozoan infections, especially with G. duodenalis and
E. histolytica/dispar infections and these rates have not indicated any
sustainable reduction since the 1980s. Besides the high rates of
infections, not much is known about factors contributing to the
high prevalence. Therefore, the present study is a cross-sectional
study aimed at determining prevalence and factors associated with
the high prevalence of intestinal protozoan infections in Yemen.
This study will assist in understanding the mode of transmission as
well as to accommodate human health practices, which opposes
the transmission of protozoan infections. Indeed, identifying
predictors of intestinal protozoan infections is crucial for the
effective implementation of control strategies in combating these
intestinal protozoan infections.
Materials and Methods
Study area and study population
This study was conducted among outpatients at Al Jomhury
hospital, Al-Kuwait hospital and Alzahrawy clinical center in
Sana’a city, Yemen. Faecal samples were collected from patients
referred to the parasitological lab for stool examination. A total of
503 samples were collected. Patients were invited to participate
voluntarily after a clear explanation of the objectives of the study
was provided and written consent obtained. If the patients were
children, written informed consents were obtained from their
parents. The study protocol was approved by the research and
ethical committee of Faculty of Medicine, University of Malaya,
Malaysia (MEC RF. No: 782.9). Permission was obtained from the
hospital authorities before the commencement of the study.
Questionnaire
Prior to sample collection, a brief explanation of the aims of
study was given to all patients who voluntarily participated.
Information was collected through a pre-tested standard question-
naire which included socio demographic information such as age,
gender, education, residence, education level, occupation and
Figure 1. Map of Yemen indicating the location of major cities and governorates.
doi:10.1371/journal.pone.0022044.g001
Intestinal Protozoa among Patients in Sana’a City
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monthly income [range from ,20000 Ryal Yemeni (,100USD)
to .20000 Ryal Yemeni (.100USD)], health practices (i.e.,
personal awareness of food and water handling beside adoption
of health hygiene) and behavioral habits (i.e., washing hands
before eating, washing hands after defecation, eating with hands,
washing fruits and vegetables and taking bath at least twice a
week), health conditions with history of symptoms (e.g., diarrhea,
nausea, vomiting and abdominal pain). Environmental conditions
such as water supply, provision of sanitation system and existence
of animal in households were also included. Age of participants
was categorized into two groups that were below 12 years and
above 12 years according to a previous study [13].
Faecal collection and examination
The stool samples were collected from patients in wide mouthed
screw-capped containers and labeled. Primary detection of
(oo)cysts and ova were made by examination of direct smear,
which was prepared from fresh stool. Wet mount preparation after
formal ether concentration method was also made to increase the
sensitivity of the detection using the light microscopy [14].
Cryptosporidium oocysts were detected using modified Ziehl-Neelsen
stain technique. Infected cases were treated by medical personnels
from the respective hospitals in Yemen. All samples were
examined at Al Jomhury hospital parasitological laboratory and
later preserved in potassium dichromate solution for further
investigations.
Statistical analysis
Data were analyzed using SPSS programme for windows
version 11.5 (SPSS Inc., Chicago.IL, USA). Univariate analyses
were used to investigate the association between dependent and
independent variables. The significance was defined as p,0.05.
Those variables that showed significance with p,0.05 were used to
develop a stepwise forward logistic regression model.
Results
A total of 503 samples were collected from patients attending
different hospitals and health center, in Sana’a City, which were
referred to a parasitological laboratory for faecal examination. Of
these patients, 219 were males and 284 were females. The age of
participants was between 1 and 80 years old. The overall
prevalence of parasitic infection was 40.3%. Multiple infections
were registered at 11.7%, with 30.9% of protozoan infection. The
prevalence of each parasite is indicated in Table 1. Giardia
duodenalis had the highest infection rate (17.7%) followed by
Entamoeba histolytica/dispar (17.1%). Other intestinal parasites
detected include Ascaris lumbricoides (2.4%), Hymenolepis nana
(1.4%), Enterobius vermicularis (0.4%) and Schistosoma mansoni (0.3%).
Univariate analysis identified six factors associated with
intestinal protozoan infections (Table 2) which include contact
with animals (OR = 1.75, 95% CI 1.17–2.62), not washing fruits
and vegetables before eating (OR = 1.66, 95% CI 1.060–2.601),
drinking untreated water (OR = 1.50, 95% CI 1.01–2.25), taking
bath less than twice a week (OR = 1.82, 95% CI 1.19–2.78),
watering plants using untreated water (OR = 1.85, 95% CI 1.07–
3.21) and working mother (farmers) (OR = 2.26, 95% CI 1.22–
4.17). Those living in the rural areas (OR = 1.52, 95% CI 0.99–
2.305) and do not practice hand washing (OR = 1.47, 95% CI
0.99–2.17) had higher infection rate. Multivariate analysis using
forward stepwise logistic regression confirmed contact with
animals (OR = 1.75, 95% CI 1.17–2.62) and taking bath less than
twice a week (OR = 1.82, 95% CI 1.19–2.78) as significant risk
factors of intestinal protozoan infections.
In addition, univariate analysis was also carried out based on
single infection with Giardia (Table 3) and E. histolytica/dispar
(Table 4). It was found that drinking untreated water was a
significant predictor of giardiasis (OR = 1.73. 95% CI = 1.05–
2.86). Unexpectedly, people with income #20000 Yemeni Ryal
appeared as a protective factor (OR = 0.4, 95% CI = 0.24–0.95)
(Table 3). Logistic regression analysis confirmed that drinking
untreated water was a significant risk factor of Giardia infection in
Yemen (OR = 2.09, 95% CI = 1.22–3.61).
E. histolytica/dispar infection was significantly associated with
contact with animals (OR = 2.75, 95% CI = 1.71–4.43), watering
activity (OR = 2.13, 95% CI = 1.15–3.95), taking bath less than
twice a week (OR = 1.82, 95% CI = 1.10–2.99), not washing hands
before eating (OR = 2.19, 95% CI = 1.31–3.64), living in rural
areas (OR = 1.72, 95% CI = 1.05– 2.82) and the absence of
common drainage (OR = 1.97, 95% CI = 1.09–3.54) (Table 4).
Logistic regression confirmed that not washing hands before eating
(OR = 1.98, 95% CI = 1.15–3.41) and contact with animals as
significant predictors of Entamoeba infection (OR = 3.09, 95%
CI = 1.88–5.06).
Discussion
The current findings indicated that the prevalence of intestinal
protozoan infections was 30.9% based on a single stool sampling.
This infection rate was low compared to a previous study carried
out on 37,000 outpatients in which the prevalence of intestinal
protozoa was 53% [5]. In comparison to other Mediterranean
countries, the infection rate with intestinal protozoa in this study is
higher than previous reports from Saudi Arabia among patients
seeking health care (27.8%–32.2%) [15,16], Iran (19.9%) [17,18]
and Oman (18%) [19], however lower compared to the prevalence
in Pakistan (52%) [20]. The most dominant protozoa in this study
were G. duodenalis and E. histolytica/dispar, which were rated at
17.7% and 17.1%, respectively. This finding was comparable to
the previous studies carried out in Yemen [6,10], except studies
among restaurant workers [7,8]. These differences could be
attributed to the differences in the study subjects and study areas.
Besides that, different diagnostic methods used from one study to
another should also be considered as a possible reason behind the
disparity in the infection rates [21,22]. This study showed a
significant association between low personal hygiene practices and
behavior with intestinal protozoan infections. Logistic regression
analysis indicated that people who did not take their bath at least
twice a week were at 2-fold higher risk of getting infection with
intestinal protozoa. Undoubtedly, the current water crisis
Table 1. Prevalence of intestinal parasitic infections
according to species (N = 503).
Parasite
No
Infected %
Giardia duodenalis 89 17.7%
Entamoeba histolytica/dispar 86 17.1%
Cryptosporidium 51%
Ascaris lumbricoides 12 2.4%
Schistosoma mansoni 2 0.3%
Hymenolepis nana 7 1.4%
Enterobius vermicularis 2 0.4%
Total 203 40.3%
doi:10.1371/journal.pone.0022044.t001
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contributed in some ways to the low hygienic practices in Yemen,
leading to the increase of intestinal parasitic diseases.
Yemen depends totally on ground water, which is dropping by
20–65 feet a year as reported by the World Bank [23]. Furthermore,
the Carnegie Endowment for International Peace noted that 19 of
Yemen’s 21 main aquifers were not being replenished because of
lower rainfall [24]. The impact of water quantity on the health
status has been well documented since plentiful and accessible
supplies of water do encourage better hygiene. Two review studies
which covered 84 studies in 28 countries have concluded that
quantity of water available has more impact on endemic diarrhea
cases in developing countries than water purity [25,26]. Another
study carried out in Nicaragua found that children from homes with
insufficient water supply had 34% higher infection rate of diarrhea
[27]. Water availability may also affect the frequency of hand
washing as it has been stated that a mother needs 20 liters of water
to wash her hands after using the latrine, changing a nappy, before
preparing food, eating, giving food to the infant and handling of
cooking or drinking utensils [28].
In the present study, logistic regression analysis also showed that
those people who came in contact with animals were at significant
risk in acquiring protozoan infections. This association implicated
animals as a significant source of protozoan infection in Yemen.
However, this postulation should be confirmed by further studies
which incorporate molecular tools. It is common for the rural
communities in Yemen to keep animals such as cattle, goats and
donkeys in the ground floor of the same house. Evidence of
zoonotic transmission of some intestinal protozoa, especially
Giardia and Cryptosporidium have been provided by several studies
via molecular data analysis [29,30].
With regards to Giardia infection, it has been shown to be
significantly associated with drinking untreated water. In Yemen,
Table 2. Factors associated with protozoan infections among patients seeking health care in Sana’a City.
Variables Infected% OR (95%CI)
p
value
Age (years) .12
#12
29.6
34
1
1.23(0.81–1.85)
0.33
Address Urban
Rural
28.4
37.6
1
1.52(0.99–2.31)
0.050
Gender Male
Female
29.4
32.2
1
1.14(0.78–1.67)
0.50
Income
(Yemeni Ryal)
.20000
#20000
31.4
28.9
1
0.89(0.55–1.45)
0.63
Family size ,5
$5
27.9
32.2
1
1.23(0.81–1.86)
0.34
Education Educated
Not educated
33.3
26.9
1
0.74(0.49–1.09)
0.13
Occupation Working
Not working
27. 8
32.5
1
0.80(0.53–1.213)
0.29
Sewage disposal Common drainage
Others
29.6
38.0
1
1.459(0.87–2.46)
0.15
Existence of animal No
Yes
27.3
39.6
1
1.75(1.17–2.617)
,
0.05*
Washing hands before eating Yes
No
26.5
34.6
1
1.47(0.99–2.169)
0.055
Eating raw vegetables No
Yes
31.6
31.2
1
0.98(0.61–1.59)
0.94
Eating fresh fruits No
Yes
28.7
33
1
0.82(0.56–1.19)
0.29
Washing fruits
and vegetabl es
Yes
No
29.0
40.4
1
1.66(1.06–2.601)
,
0.05
Drinking water Treated
Not treated
25.9
34.5
1
1.50(1.01–2.25)
,
0.05
Bathing two times weekly Yes
No
27.7
41.1
1
1.82(1.19–2.78)
,
0.05*
Washing hands after defecation Yes
No
28. 6
33.7
1
1.27(0.86–1.873)
0.23
Watering plants No
Yes
29.7
43.3
1
1.185(1.07–3.20)
,
0.05
Diarrhea No
Yes
29.6
33.72
1
1.28(0.81–1.80)
0.35
Father occupation Others
Farmer
35.2
29.1
1
1.32 (0.87–2.00)
0.19
Mother occupation Others
Farmer
28.9
47.8
1
2.26(1.22–4.17)
,
0.05
*Confirmed by logistic regression.
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ground water is the main source of drinking water. Given that
most of the homes are without a proper sanitary system, the
possibility of faecal contamination is high via ground seepage [31].
Furthermore, it was noted that people in rural areas are dependent
on dams besides wells as drinking water resources. Dam water is a
collection of rainwater, which is exposed to high pollution,
especially during the rainy season due to soil runoff contaminated
with parasite (oo)cysts and ova from animal and human faeces.
Previously, the using of well water has been identified as significant
predictors of E. histolytica and Giardia infections in Saudi Arabia.
Comparatively, those who use desalinated water have the lowest
degree of exposure to the risk of infection [32]. Contamination of
drinking water with Giardia cyst during transporting and storing of
drinking water are highly possible as rural people in Yemen use
containers to transfer water from the dams or wells to the houses
where water is stored to be used for drinking and cooking. Faecal
contamination of drinking water between the source and the point
of use is well known [33] and improving household water
management has been promoted as low cost health intervention
to combat waterborne infections [34].
As for E. histolytica/dispar infection, the present findings showed
that those who do not practice proper hand washing before eating
was at two fold higher risk of acquiring E. histolytica/dispar
infection. The major role of contaminated hands in the faecal-
oral transmission of diseases has been well documented in
developing countries and washing hands before eating or after
defecation has been considered as a secondary barrier. In
Indonesia, it has been reported that people who never or
sometimes wash hands had a four times higher risk of getting
severe diarrhea [35]. In Nepal, the practice of hand washing had a
strong correlation with the prevalence of parasitic infection [36].
Another case-control study in the same country indicated that
Table 3. Factors associated with G. duodenalis infection among patients seeking health care in Sana’a City.
Variables Infected% OR (95%CI)
p
value
Age (years) .12
#12
16.8
20.1
1
1.25(0.77–2.05)
0.37
Address Urban
Rural
16.1
21.8
1
1.45(0.88–2.39)
0.14
Gender Male
Female
15.6
19.4
1
1.31(0.82–2.09)
0.27
Income
(Yemeni Ryal)
.20000
#20000
19.5
10.3
1
0.47(0.24–0.95)
,
0.05
Family size ,5
$5
17.8
17.5
1
1.02(0.62–1.68)
0.94
Education Educated
Not educated
19.1
15.2
1
0.76(0.47–1.23)
2.26
Occupation Working
Not working
18.8
15.2
1
0.77(0.46–1.29)
0.33
Sewage disposal common drainage
Others
17.1
21.1
1
1.31(0.70–2.44)
0.40
Existence of animal No
Yes
17.7
18.0
1
1.10(0.67–1.81
`
1
0.70
Washing hands before eating Yes
No
18.0
17.7
1
0.98(0.61–1.56)
0.92
Eating raw vegetables No
Yes
15.8
18.2
1
1.18(0.64–2.17)
0.59
Eating fresh fruits No
Yes
16.7
18.9
1
0.86(0.54–1.36)
0.52
Washing fruits
and vegetabl es
Yes
No
17.4
20.2
1
0.86(0.54–1.37)
0.51
Drinking water Treated
Not treated
13.2
20.8
1
1.73(1.05–2.86
,
0.05*
Bathing two times weekly Yes
No
16.0
20.8
1
1.60(0.97–2.64)
0.06
Washing hands after defecation Yes
No
16.1
20.3
1
1.33(0.83–2.12)
0.20
Watering plants No
Yes
17.0
23.3
1
1.49(0.78–2.84)
0.23
Diarrhea No
Yes
15.9
21.7
1
1.47(0.92–2.35)
0.11
Father occupation Others
Farmer
19.3
16.7
1
1.19(0.72–1.98)
0.49
Mother occupation Others
Farmer
16.3
26.5
1
1.78(0.88–3.61)
0.10
*Confirmed by logistic regression.
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people who never used soap for washing hands were at 30 times
higher risk of typhoid [37]. In addition, not washing hands has
been reported to be significantly associated with diarrhea in
Malaysia [38] and Myanmar [39]. Intervention trials and case-
control studies, conducted in Bangladesh, have also indicated that
not washing hands was a significant risk for diarrhea [40,41,42].
In addition, animal contact was also identified as a significant
factor associated with Entamoeba infection. Although it is still
unclear whether Entamoeba infection is zoonotic or not, this
parasite has been isolated from animals. In Ethiopia, a study on
baboon and Cercopithecus (old world monkey) found that the
prevalence of E. histolytica was 24.4% [43]. Another study carried
out in Ethiopia found that cockroaches serve as carriers of human
intestinal parasites [44]. In Uganda, E. histolytica and Giardia have
been detected in monkeys [45]. Similarly, in the Philippines, E.
histolytica and E. dispar were detected among captive macaques in a
primate facility. In the same study, using PCR, they found that 23
E. histolytica isolates were identical to human E. histolytica [46]
highlighting a possibility of zoonotic transmission.
In conclusion, the present study showed high prevalence of
intestinal protozoan infections with E. histolytica/dispar and G.
duodenalis being the most predominant protozoa among patients
seeking health care in Yemen. Low personal hygiene practices
such as not washing hands before eating and the frequency of
bathing, besides water contamination seemed to play major roles
in the high transmission of intestinal protozoa. Therefore, these
factors should be given due consideration when implementing any
interventions to combat these intestinal protozoan diseases.
Although animals are still a possible source of human infection
with protozoa as shown in this study, this postulation warrant
further studies especially those that utilize advanced molecular
techniques. Genotyping E. histolytica/dispar and G. duodenalis from
Table 4. Factors associated with E. histolytica/dispar infection among patients seeking health care in Sana’a City.
Variables Infected% OR (95%CI) p value
Age (years) .12
#12
15.5
18.8
1
1.17(0.71–1.93)
0.54
Address Urban
Rural
15.0
23.3
1
1.72(1.05–2.82)
,
0.05
Gender Male
Female
17.9
16.6
1
0.91(0.57–1.45)
0.71
Income
(Yemeni Ryal)
.20000
#20000
17.5
17.0
1
1.04(0.58–1.86)
0.91
Family size ,5
$5
19.3
12.3
1
1.69(0.98–2.93)
0.06
Education Educated
Not educated
16.3
17.8
1
1.07(0.67–1.71)
0.26
Occupation Working
Not working
17.9
16.5
1
0.90(0.55–1.50)
0.33
Sewage disposal Common drainage
Others
15.6
26.8
1
1.97(1.10–3.55)
,
0.05
Existence of animal No
Yes
12.5
28.2
1
2.75(1.71–4.43)
,
0.05*
Washing hands before eating Yes
No
11.4
21.9
1
2.19(1.31–3.64)
,
0.05*
Eating raw vegetables Yes
No
16.9
20.0
1
0.81(0.46–1.43)
0.47
Eating fresh fruits No
Yes
16.7
18.9
1
0.86(0.54–1.37)
0.52
Washing fruits
and vegetabl es
Yes
No
15.6
24.0
1
1.71(1.01–2.89)
,
0.05
Drinking water Treated
Not treated
13.2
19.9
1
1.63(0.98–2.69)
0.06
Bathing two times weekly Yes
No
14.9
24.2
1
1.82(1.10–2.99)
,
0.05
Washing hands after defecation Yes
No
15.2
18.8
1
1.29(0.80–2.09)
0.29
Watering plants No
Yes
15.6
28.3
1
2.13(1.15–3.95)
,
0.05
Diarrhea No
Yes
15.7
18
1
0.85(0.51–1.40)
0.52
Father occupation Others
Farmer
15.2
22.8
1
2.33(1.18–4.59)
,
0.05
Mother occupation Others
Farmer
15.8
30.4
1
1.97(1.10–3.55)
,
0.05
*Confirmed by logistic regression.
doi:10.1371/journal.pone.0022044.t004
Intestinal Protozoa among Patients in Sana’a City
PLoS ONE | www.plosone.org 6 July 2011 | Volume 6 | Issue 7 | e22044
human, animals and water resources are highly recommended to
understand the actual dynamics of transmission of these protozoa
in Yemen. Likewise, the authority must take into consideration the
development of health awareness among the community through
active encouragement of individuals in adopting hygienic
behaviors via audio, visual and curriculum programs. Radical
solution to water scarcity is also an important requirement to
combat the proliferation of these infections in Yemen.
Acknowledgments
The authors would like to thank the staff of Al Jomhury hospital, Al-
Kuwait hospital and Alzahrawy clinical center for their kind assistance.
Author Contributions
Conceived and designed the experiments: NAA MAKM RM YALL.
Performed the experiments: NAA. Analyzed the data: NAA. Contributed
reagents/materials/analysis tools: NAA MAKM RM YALL. Wrote the
paper: NAA.
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Intestinal Protozoa among Patients in Sana’a City
PLoS ONE | www.plosone.org 7 July 2011 | Volume 6 | Issue 7 | e22044
    • "Similarly, it is also worth noting that knowledge about the symptoms of schistosomiasis among the respondents was negligible, as only 22.88 % of them mentioned diarrhea and 21.95 % blood in stools. This could be attributed to the disease being frequently confused with other intestinal infections exhibiting similar symptoms, such as amoebic dysentery, which is common among the targeted populations [10, 11]. The theoretical foundation in the Health Belief Model (HBM), integrates people's knowledge, perceptions, attitude and practices to a disease in establishing trends of infection [12]. "
    [Show abstract] [Hide abstract] ABSTRACT: Background Schistosomiasis remains a major public health problem in Kenya. Inadequate knowledge, attitudes and practices (KAP) on causative factors are some of the critical factors for the increased prevalence. The study assessed KAP on the control and prevention of schistosomiasis infection in Mwea division, Kirinyaga County-Kenya. Four hundred and sixty five house-hold heads were enrolled in this study by use of simple random sampling technique. Methods The study employed an analytical descriptive cross sectional design utilizing both quantitative and qualitative data collection methods. A pretested structured questionnaire, Focus Group Discusions (FGDs) and Key Informant Interviews (KII) guides were used for data collection. Descriptive statistics and Chi square tests and Fisher’s exact tests were computed where applicable. Data from the FGDs and KIIs were analyzed using NUID.IST NUIRO.6 software. ResultsSignificant associations between knowledge and demographic factors i.e. age (p = 0.011), education level (p = 0.046), were reported. Handwashing after visiting the toilet (p = 0.001), having a toilet facility at home (p = 0.014); raring animals at home (p = 0.031), households being affected by floods (p = 0.005) and frequency of visits to the paddies (p = 0.037) had a significant association with respondents practices and schistosomiasis infection. Further significance was reported on households being affected by floods during the rainy season (p < 0.001), sources of water in a household (p < 0.047) and having a temporary water body in the area (p = 0.024) with increase in schistosomiasis infection. Results revealed that respondents practices were not significantly associated with gender (p = 0.060), marital status (p = 0.71), wearing of protective gear (p = 0.142) and working on the paddies (p = 0.144). Conclusions This study reveals that knowledge about the cause, transmission, symptoms and prevention of schistosomiasis among the Mwea population was inadequate, and that this could be a challenging obstacle to the elimination of schistosomiasis in these communities. Due to various dominant risk factors, different control strategies should be designed. Therefore, there is a need for integrated control programme to have a lasting impact on transmission of schistosomiasis infection. Control programs like mass drug administration need to go beyond anti-helminthic treatment and that there is a need of a more comprehensive approach including access to clean water, sanitation and hygiene. School and community-based health education is also imperative among these communities to significantly reduce the transmission and morbidity from schistosomiasis.
    Full-text · Article · Dec 2016
    • "The unexpectedly low prevalence of T. trichiura in the present study is lower than those recently reported among children from Ibb and Al-Mahweet, being 9.3% and 18.0%, respectively (Alsubaie et al., 2016; Alwabr and Al-Moayed, 2016). On the other hand, the absence of hookworms and S. stercoralis among schoolchildren in the present study is consistent with other previous studies (AlQobati et al., 2012; Al-Shibani et al., 2009b; Alyousefi et al., 2011; Azazy and Al-Tiar, 1999; Azazy and Raja'a, 2003; Bin Mohanna et al., 2014). However, low prevalence rates of 1.2% and 0.8%have been recently reported for hookworms and S. stercoralis, respectively, among schoolchildren in Ibb (Alsubaie et al., 2016). "
    [Show abstract] [Hide abstract] ABSTRACT: Yemen is a developing country overwhelmed with a triad of poverty, diseases and social conflicts. Moreover, the majority of its population live in rural communities and suffer from intestinal parasitic infections (IPIs). Therefore, the present school-based, cross-sectional survey aimed to detect the prevalence of such infections and associated risk factors among schoolchildren in the rural communities of Bani Alharith, Hamdan and Bani Hushaysh districts of Sana'a, north of Yemen. Socio-demographic data and certain behavioral risk factors as well as stool samples were collected from 1218 schoolchildren from ten randomly schools in the study area. Fresh stool samples were examined for parasites by direct saline and iodine preparations and after concentration with formol-ether technique. The overall prevalence of IPIs was 54.8%, with a higher frequency of protozoal than helminthic infections (37.6 vs. 17.2%, respectively). Parasite species recovered were Entameba histolytica (21.5%), Giardia lamblia (16.1%), Ascaris lumbricoides (8.3%), Hymenolepis nana (5.3%), Schistosoma mansoni (2.6%), Trichuris trichiura (0.5%) and Enterobius vermicularis (0.4%). Univariate analysis showed that the male gender and illiteracy of fathers and/or mothers were the socio-demographic factors significantly associated with higher infection rates. The illiteracy of mothers was also confirmed as an independent risk factor by multivariable analysis. On the other hand, not washing hands before eating, not washing fruits and vegetables before consumption, eating uncovered food and not clipping fingernails were the risk behaviors significantly associated with higher infection rates, with the last three ones being confirmed as independent risk factors. Therefore, control measures should include regular treatment of protozoal infections and deworming of schoolchildren, promotion of hygiene in rural schools through health education programs, regular inspection of schoolchildren for personal hygiene practices and the provision of a healthy school infrastructure.
    Full-text · Article · Aug 2016
    • "It is also more prevalent than in other Middle Eastern countries, such as Syria (0.01%) [36], Qatar (0.3%) [58] and Iran (0.4–2%) [59,60], and in other developed [37] and developing countries [61]. Nevertheless, the parasite is less common than in other developing countries like Pakistan (14%) [38], Yemen (17%) [49], and India (18%) [62]. In a recent study to assess the prevalence and genetic diversity of E. histolytica in individuals with gastrointestinal symptoms in a rural area of southern Ethiopia, a prevalence of 3.3% was found [63]. "
    Full-text · Article · Apr 2016
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