Jeannine et al Journal of Drug Delivery & Therapeutics.

2024; 14(5):102-107

Available online on 15.05.2024 at http://jddtonline.info

Journal of Drug Delivery and Therapeutics

Open Access to Pharmaceutical and Medical Research
Copyright © 2024 The Author(s): This is an open-access article distributed under the terms of the CC BY-NC 4.0 which
permits unrestricted use, distribution, and reproduction in any medium for non-commercial use provided the original
author and source are credited

Open Access Full Text Article Research Article

Soil-Transmitted Helminthiasis, Intestinal Schistosomiasis and Malaria Co-

Infections among Children in Rural Communities Around Rwasave and
Cyarwa Valleys
UWIMANA Jeannine 1,3*, ISHIMWE Alain Prudence 1,2, MUTESA Leon 2, NTEZIRIZAZA Evariste 1,3, TUYISHIME
Jean de Dieu 1
1: Ines-Ruhengeri, Faculty of Applied Fundamental Sciences, Department of Biomedical Laboratory Sciences, Rwanda
2: University of Rwanda, College of Medicine and Health Sciences, Rwanda
3: Kigali University Teaching Hospital, Rwanda

Article Info: Abstract

___________________________________________ ___________________________________________________________________________________________________________________
Article History:
Background: Soil-transmitted helminthiasis, schistosomiasis and malaria remain a threat in
Received 12 March 2024 developing countries, especially to people living in rural areas near large water bodies, valleys or
Reviewed 14 April 2024
Accepted 02 May 2024
swamps whose daily life activities revolve around those areas. In addition, these parasites affect
Published 15 May 2024 different groups of people especially those in contact with their breeding sites including children
mostly due to their developing immunity compared to that of old people.
__________________________________________
Cite this article as: Methodology: This cross-sectional study was conducted in rural communities near the Rwasave and
Cyarwa valleys, with 124 school-aged children participating. Stool samples were tested for the
Jeannine U, Alain Prudence I, Leon M, Evariste N,
Jean de Dieu T, Soil-Transmitted Helminthiasis,
presence of STH eggs and intestinal Schistosoma parasites using the Kato Katz technique, and thick
Intestinal Schistosomiasis and Malaria Co- blood smears were made to aid in the identification of plasmodium species in blood. The threshold
Infections among Children in Rural Communities intensity of infection on STHs and Schistosoma sp. was estimated by counting their eggs
Around Rwasave and Cyarwa Valleys, Journal of microscopically, which aided in classifying infections as light, moderate, or heavy according to WHO
Drug Delivery and Therapeutics. 2024; standards. Furthermore, Plasmodium species were identified by the presence of schizonts,
14(5):103-107 trophozoites, or gametocytes on Giemsa-stained thick blood smears, and parasitic density was
DOI: http://dx.doi.org/10.22270/jddt.v14i5.6613 calculated as a result.
___________________________________________ Results: In this study, the highest prevalence of soil transmitted helminthiasis was 12.7% in Cyarwa
*Address for Correspondence: valley compared to 12.5% in Rwasave valley. The highest prevalence of Schistosomiasis was 3.2% in
UWIMANA Jeannine,
Cyarwa valley compared to 1.3% in Rwasave valley. Prevalence of malaria in Cyarwa valley was 3.3%
in 63 children. Where children infected were only males falling in 5-8 age group.
Ines-Ruhengeri, Faculty of Applied Fundamental
Sciences, Department of Biomedical Laboratory Conclusion: Results showed high prevalence of soil transmitted helminthiasis which was 12.7% in
Sciences, Rwanda. Cyarwa compared to 12.5% in Rwasave valley especially in children aged 5-8, this due to poor
Kigali University Teaching Hospital, Rwanda sanitation (P<0.001) that have assessed. Surprisingly, Cyarwa valley is located nearby town. Whereas
malaria, intestinal schistosomiasis was low and there were not significantly associated with their risk
factors with p-values 0.4, 0.092 respectively which can show that, preventive measures that have been
established by government of Rwanda have positive impacts. Furthermore, there was a low
prevalence of soil transmitted helminthiasis, intestinal schistosomiasis and malaria co-infection.
Keywords: soil transmitted helminthiasis, intestinal schistosomiasis, malaria.

INTRODUCTION respectively2. Preschool and school-going children carry the

highest burden with data showing that above 270 million
Soil-transmitted helminthiasis, schistosomiasis and malaria preschool children and above 600 million school-going children
remain a threat in developing countries, especially to people are infected2. In Rwanda, A national survey conducted in 2008
living in rural areas near large water bodies, valleys or swamps showed that over 8000 school children and 66% of children
whose daily life activities revolve around those areas1. In were infected with soil-transmitted helminths3.
addition, these parasites affect different groups of people
especially those in contact with their breeding sites including Schistosomiasis is one of the neglected tropical diseases caused
children mostly due to their developing immunity compared to by Schistosoma species4. Worldwide schistosomiasis causes
that of old people2. morbidity among people with an estimated 230 million and
200,000 deaths occurring annually2.In Rwanda, a survey done
Soil-transmitted helminths pose serious public health among 270 school-aged children and adults showed a
challenges worldwide, affecting more than 1.75 billion people, schistosomiasis prevalence of 20.1%3. Generally, these findings
with 471 million, 477 million and 804 million infected with highlight the high prevalence of Schistosoma mansoni
hookworms, Trichuris trichiura and Ascaris lumbricoides
ISSN: 2250-1177 [102] CODEN (USA): JDDTAO
Jeannine et al Journal of Drug Delivery & Therapeutics. 2024; 14(5):102-107

transmission in Rwanda and the prevalence of the infection children living around the Rwasave and Cyarwa valleys of the
varies from one epidemiological setting to another3. southern province of Rwanda.
Malaria is a life-threatening disease caused by plasmodium Study Population
species and it is transmitted via an infected female anopheles
The current study involved participants aged 5-12 years lived
mosquito bite5. Reports from WHO indicated 241 million cases
in rural communities near Rwasave and Cyarwa valleys.
of malaria in 2020 with children under five years old
accounting for almost 80% of all malaria deaths6. In Rwanda, a Sampling technique
study conducted by Rudasingwa & Cho7, in 2020 showed that
7.4 % of 3180 children were infected. However, there was a A convenient sampling strategy was used in this study. This
reduction in incidence from 400 to 148 per 1000 in 20208. non-probability sampling technique included all participants
aged 5-12 years old available and willing to participate during
Soil-transmitted helminthiasis and schistosomiasis are the time of the study until the sample size was achieved.
classified into a group of neglected tropical diseases2. These
parasites have shown co-infection with a prevalence of 6% in Data collection methods and procedures
2020 by Jean Claude et. Al9 in school-aged children. However, A structured questionnaire was used for the collection of socio-
the literature related to this co-infection in Rwanda remain demographic information and possible risk factors associated
uncommon. Although schistosomiasis and malaria co-infection, with the infections including poor sanitation, access to clean
are believed to be the major parasitic diseases of the tropics water, wearing shoes, and the use of bed nets. To diagnose STHs
causing morbidity and mortality out of the 825 infected and Schistosoma infections in stool specimens, children’s
children1, different studies in Rwanda reported the prevalence parents or their guardians were given labelled plastic stool
of different parasites and their burden on the country but there containers and instructions by a research team on how to
is limited data on the prevalence of co-infections. collect a portion of their morning stool samples a day before the
Soil-transmitted helminths and malaria co-infection prevalence parasitological screening. Then, stool samples were collected
are estimated high in children living in endemic countries1,10 by a member of the research team the following day and
and an overall prevalence of plasmodium-helminths co- brought to Rango Health Center Laboratory for analysis. A
infections reported was 17.7%10. In Rwanda, a study conducted direct wet mount stool examination was performed
by Marcelline et.al in 2016 reported that the overall prevalence immediately by emulsifying a small portion of the stool sample
of malaria, helminthiasis and anaemia was 30.8%, 47.5% and with normal saline for microscopic examination using light
30.1% respectively, with helminthiasis estimated to be more microscopy. In addition, a Kato-Katz cellophane thick smear
prevalent among 6- to 10-year-old children and its co-infection was made from each sample and examined immediately to
with malaria was 61.5%5. avoid the disappearance of the helminthic eggs due to
deterioration. To determine the threshold intensity of infection,
Schistosomiasis, soil-transmitted helminthiasis, and malaria the mean number of eggs counted per gram of faeces, from each
are reported to be triple threats in preschool and school-going Kato Katz thick smear was multiplied by 50 because a Kato Katz
children1. A study conducted in 2010 determined the template of 20 mg was used. Following the WHO standard
prevalence of Plasmodium falciparum-malaria, intestinal procedure, infection intensity was classified as light, moderate,
schistosomiasis, soil-transmitted helminth infections, and their or heavy for common STHs infections13. Laboratory procedures
respective co-infections among school-going children and were carried out following standard operating procedures.
found that the prevalence of co-infection of Plasmodium Stool samples were chosen at random for quality control and
falciparum, Schistosoma mansoni and hookworm was 2.8%11. In examined by a third person who was not aware of the previous
Rwanda, there is limited availability of data on the prevalence test results.
of polyparasitism especially those which are classified as
neglected tropical diseases. For malaria diagnosis, a finger pricks blood sample was
collected after cleaning the finger surface using an alcohol swab
Generally, Helminthiasis, Schistosomiasis and malaria affect (70% isopropanol-impregnated swabs) on the same day of
poor people living in rural and peri-urban settings with limited collecting stool specimens. One thick smear was produced and
access to clean water, and inadequate sanitation and hygiene stained with a newly prepared 10% Giemsa working solution
services1. In addition, people living near irrigation sites, dam (prepared after filtration of stock solution) in phosphate-
areas, those who rear livestock near rivers, and also those who buffered water (pH 7.2). Parasite density was estimated under
don’t use mosquito nets during the night, are at high risk of a light microscope at high magnification by counting the
being infected with malaria12. The present study, therefore, was number of parasites per 200 white blood cells (WBC). If < 100
aimed to determine the prevalence of soil-transmitted parasites were found, the reading continued up to 500 WBC14.
helminths, Schistosoma, and Malaria co-infections among 5-12 The determination of a plasmodium species is made with
years old children living around the Rwasave and Cyarwa certainty by the presence of trophozoites, schizonts or
valleys of the southern province of Rwanda. Furthermore, gametocytes. However, no speciation was done as this study
understanding the degree of polyparasitism in high-risk groups emphasized only the presence or absence of plasmodium
will aid in the development of effective intervention measures species and parasitic density. The following formula was used
to minimize disease burden and co-morbidity. to calculate parasite density:
METHODOLOGY
Study area
Data analysis
The present study was conducted in rural communities living
around Rwasave and Cyarwa valleys. After verifying the structured questionnaire completeness, data
were entered into a Microsoft Excel database, version 2016
Study Design (16.0.4266.1001 version) and then, the data collected were
A cross-sectional study design was used in this study to imported into SPSS analyzing tool version 22.0.0.0 for
determine the prevalence of soil-transmitted helminths, statistical analysis to calculate percentages, and descriptive
Schistosoma, and Malaria co-infections among 5-12 years old statistics (i.e. mean, standard deviation, etc.) and to design
tables. The prevalences were expressed in all sites and were

ISSN: 2250-1177 [103] CODEN (USA): JDDTAO

Jeannine et al Journal of Drug Delivery & Therapeutics. 2024; 14(5):102-107

stratified by gender and age bands of 5-8 and 9-12 years. The Children from cyarwa
P-value was calculated to determine the correlation between 25
parasites and socio-demographic variables and a P-value of
20
<0.05 was considered statistically significant in all
comparisons. Chi-squared (X2) tests were used to assess the 15

counts
association of variables such as mixed infections (single and
double or triple parasitic infections) with demographics. The t- 10 F
test was used to compare the mean difference in STHs,
5 M
Schistosoma infection intensity and plasmodium sp. density
between the Cyarwa and Rwasave valleys. results were
0
presented using tables, charts and graphs.
5-8 9-12
RESULTS Ages in years

Participants information Figure.4.2. children from cyarwa

This study enrolled 143 children of which 76 (53.1%) were Prevalence of soil-transmitted helminths, intestinal
males and 67 (46.9%) were females. Among them, 80(55.9%) schistosomiasis, malaria parasite and their coinfections.
children were from rural communities near the Rwasave valley
This study reported a high prevalence of single or mixed
and 63 (44.1%) lived near Cyarwa valley. Study participants
infection of soil-transmitted helminths in communities near
were aged 5 to 12 years old, with a mean age of 8.13 (n=143,
Rwasave valley with 12.5% (n=11, 95%CI: 0.0621-0.2129),
SD=2.31) years and were all born or lived near those valleys
whereas intestinal schistosomiasis, and malaria infection were
which they recruited from more than six months.
1.3% (n=1, 95%CI:-0.0118-0.0368), and 0%(95%CI:0) in
Children form rwasave school-aged children respectively. Contrarily, the community
25 around Cyarwa had a prevalence of 12.7%(n=7, 95%CI: 0.107-
0.113) for single or mixed infection of STHs, 3.2%(n=2, 95%CI:-
20 0.01142-0.07482) for intestinal schistosomiasis, and
15 3.3%(n=2, 95%CI: 0.012-0.072) for malaria infection. In
counts

addition, the low prevalence of double co-infection was

10 F observed primarily in communities near Cyarwa, with
5 M 1.6%(n=1, 95%CI: -0.015-0.045) of both STHs-Malaria and
Schistosomiasis-malaria co-infections recorded. However,
0 STHs & Schistosomiasis, on the other hand, did not co-infect.
5-8 9-12 Furthermore, none of the participants were infected with all
Age in years three infections. On the other hand, only 1.3%(n=1, 95%CI: -
0.0118-0.0368) of communities near Rwasave had of co-
Figure. 4.1. children from regions around rwasave infection with STHs and Schistosomiasis, and also no co-
infection with all three infections recorded.
-and as(See table 4.1.).

Table 4.1. shows Prevalence of soil transmitted helminths, intestinal schistosomiasis, malaria and their co-infections.
Prevalence of single and multiple infections
RWASAVE (N=80) CYARWA (N= 63)
Prevalence Prevalence
Single infection n (%) 95% C.I n (%) 95% C.I
Malaria 0 0% 0-0 2 3.3% 0.012-0.072
STHs 11 12.5% 0.0621-0.2129 7 12.7% 0.107-0.113
Intestinal schistosoma sp 1 1.3% -0.0118-0.0368 2 3.2% -0.01142-0.07482
Co-infections
Malaria and STHs 0 0% 0-0 1 1.6% -0.015-0.045
Malaria and intestinal schistosoma sp 0 0% 0-0 1 1.6% -0.015-0.045
STHs and intestinal schistosoma sp 1 1.3% -0.0118-0.0368 0 0% 0-0

intestinal schistosoma sp and STHs

and Malaria 0 0% 0-0 0 0% 0-0

ISSN: 2250-1177 [104] CODEN (USA): JDDTAO

Jeannine et al Journal of Drug Delivery & Therapeutics. 2024; 14(5):102-107

Risk factors associated with soil-transmitted helminths, not sleeping under mosquito nets was not a significant factor to
intestinal schistosomiasis, plasmodium parasites and their get malaria infection (n=2, p=0.4) in children near both
coinfections. Rwasave and Cyarwa valleys. The occurrence of co-infection
(n=1, p=0.067) of STHs and Malaria as well as STHs-
School-aged children who did not practice washing their hands
Schistosomiasis and Schistosomiasis-Malaria recorded in
before eating, walking barefoot, or fetching water in the valley
children walking barefoot, fetching in the valley, hand washing
had the highest likelihood of becoming infected with soil- and not sleeping under mosquito-nets were statistically
transmitted helminths, with an odd ratio of 14 (P=0.0001).
insignificant However, no risk factor associated with co-
However, those factors were insignificant in children to get
infection with all three infections because there was no case
infected with Intestinal schistosomiasis (n=3, p<0.092). Also,
recorded (Table. 4.2).

Table 4.2. Risk factors associated soil transmitted helminths, intestinal schistosomiasis, plasmodium parasites and their coinfections.
Characteristics of participants

STH and Malaria

MALARIA (n=2)

Schistosomiasis

Schistosomiasis
schistosomiasis
overall(n=143)

and Malaria
STH (n=18)
risk factors

Intestinal

P VALUE

P VALUE
STH and
P Value

P Value

P Value

P Value
(n=3)

(n,(%)) (n,(%)

Hand-
washing
2 0.09
yes 88 (61.5%) 2 (2.3%) (2.3%) 2 2 (2.3%) 0 (0%)
16 <0.00 1 1 0.06 0.06
no 55 (38.5%) (29.1%) 1 (1.8%) 0 (0%) (1.8%) 7 1 1 1 7

Wearing-
shoes
always
yes 58 (40.6%) 4 (6.9%) 0 (0%) 1 (1.7%) 0 (0)
14 <0.00 3 0.09 1 1 0.06 0.06
no 85 (59.4%) (16.5%) 1 (3.5%) 2 (1.2%) (1.2%) 7 1 1 1 7

Mosquito
-nets
17 <0.00 2
yes 79 (55.2%) (21.5%) 1 (2.5%) 0 (0%) 0 (0%)
1 1 0.06 0.06
no 64 (44.8%) 1 (1.6%) (1.5%) 2 (3.1%) 0.4 (1.5%) 7 1 1 1 7
Fetching
valley
water
139 18 <0.00 2 1 1 0.06 0.06
yes (97.2%) (12.9%) 1 (1.4%) (0.7%) (0.7%) 7 1 1 1 7
no 4 (2.8%) 0 (0%) 1 (25%) 1 (25%)

key: p value is significantly considered when is less than 0.05 hence based on the above table STH was significantly associated with risk factors of
handwashing factor where among 18 children infected 16 were not able to wash their hands after using latrines. confidence level (95%)

The intensity of soil-transmitted helminths, intestinal near Rwasave and the lowest mean intensity of 420 eggs/gram
schistosomiasis and Plasmodium species. seen in Cyarwa. Schistosomiasis mean intensity for Rwasave
and Cyarwa were 150 eggs/gram and 200 eggs/gram
The overall mean intensity of soil-transmitted helminthiasis
respectively with an overall intensity of 166.7 eggs/gram.
recorded was 457.5 eggs/gramof faeces with the highest mean
However, the overall mean parasite density for malaria was
intensity of 495 eggs/gram of faeces in school aged children
420 parasites/µl of blood.

ISSN: 2250-1177 [105] CODEN (USA): JDDTAO

Jeannine et al Journal of Drug Delivery & Therapeutics. 2024; 14(5):102-107

Table 4.3. The intensity of soil-transmitted helminths, intestinal schistosomiasis and Plasmodium species.
Variables Infection status Cyarwa Rwasave P value
STHs (Mean) Light 8 10 0.962
Moderate 0 0
Heavy 0 0
Schistosomiasis Light 0 0 0.962
Moderate 2 1
Heavy 0 0
Plasmodium Low 2 0
High 0 0
Key: According to WHO13 soil-transmitted helminth infection is considered light, moderate and heavy when they are (1-4999, 5000-49999,>50,000)
eggs/gram respectively. Schistosomiasis is considered a light, moderate and heavy infection when they are (1-99,100-399, >400) eggs/gram
respectively. For plasmodium the intensity(55) is measured in parasites/ µl and classified based on <1000, 1000-4999, 5000-99999, >100000
when they are low, moderate, high and hyper-parasitemia respectively. P value significant at 0.01. confidence level (95%)

DISCUSSION prevalence of soil transmitted helminthiasis and

schistosomiasis was observed in Rwasave valley which is 1.3%.
In this study, the highest prevalence of soil transmitted Children infected were only males falling in 5-8 age group This
helminthiasis was 12.7% in Cyarwa valley compared to 12.5% prevalence is low compared to 4.76% 9. This could be due to
in Rwasave valley. This infection was mainly found in males different study areas, age-groups and sample size. This study
falling in 5-8 age group and this high number could be suggested negative co-infection between soil transmitted
explained by the factor that males they are the one who mostly helminthiasis, intestinal schistosomiasis and malaria
go to the valleys compared to female as it was found to be 73,
65 male and female respectively. This is similar to those shown CONCLUSION
that pre-school and school-aged children carry the highest
prevalence of soil transmitted helminths4. And also, this Results showed high prevalence of soil transmitted
helminthiasis which was 12.7% in Cyarwa compared to 12.5%
infection was mainly found in children who didn’t prefer to
in Rwasave valley especially in children aged 5-8, this due to
wash their hands after using toilets (p <0.001) (See table 4.2).
poor sanitation (P<0.001) that have assessed. Surprisingly,
which is also similar to factors shown that those parasites are
Cyarwa valley is located nearby town. Whereas malaria,
also spread in areas with poor sanitation15.
intestinal schistosomiasis was low and there were not
The highest prevalence of Schistosomiasis was 3.2% in Cyarwa significantly associated with their risk factors with p-values 0.4,
valley compared to 1.3% in Rwasave valley. Both prevalence’s 0.092 respectively which can show that, preventive measures
were low compared to 20.1% that have found among 240 that have been established by government of Rwanda have
children 16. This discrepancy could be due to different age positive impacts. Furthermore, there was a low prevalence of
groups that were used. This infection was found in males and soil transmitted helminthiasis, intestinal schistosomiasis and
female falling in both age groups 5-8 & 9-12. Also, malaria co-infection.
schistosomiasis has been found in children who are exposed to
valley, fetching valley’s water and those who likely went to the Acknowledgments
valley with bare feet (P=0.092) (See table 4.2). these factors are We extend our gratitude to the University of Rwanda, Rango
similar to those shown 4 that when your skin is in contact with Health Center and Kabutare District Hospital for facilitating this
contaminated freshwater, you are risky of being infected. study at their health facilities.
Prevalence of malaria in Cyarwa valley was 3.3% in 63 children.
Where children infected were only males falling in 5-8 age
Conflict of interest
group. Surprisingly, this prevalence was high compared to 7.4 Authors declare no conflict of interest
% of 3180 children found in 20207 . This discrepancy could be
due different study area, and age-group. Moreover, malaria Availability of raw data and material
infection was found in children who didn’t sleep under
Raw data and information on material should be obtained from
mosquito nets which is one of risk factors associated with
the corresponding author upon request.
malaria infection (P=0.4) (See table 4.2). Prevalence of malaria
and soil transmitted helminthiasis was observed in Cyarwa REFERENCES
valley which is 1.6% of 63 children. Where children infected
were only males falling in 5-8 age group. This prevalence is low 1. Afolabi MO, Ale BM, Dabira ED, Agbla SC, Bustinduy AL, Ndiaye JLA,
compared to 61.5% in 465 children from Bugesera district have et al. Malaria and helminth co-infections in children living in
endemic countries: A systematic review with meta-analysis. PLoS
shown 5 . This difference could be due to different study areas
Negl Trop Dis. 2021 Feb 1;15(2):1-26.
and age-groups. https://doi.org/10.1371/journal.pntd.0009138 PMid:33600494
Prevalence of malaria and schistosomiasis was observed in PMCid:PMC7924789
Cyarwa valley which is 1.6% of 63 children. Where children 2. Jeza VT, Mutuku F, Kaduka L, Mwandawiro C, Masaku J, Okoyo C, et
infected were only males falling in 5-8 age group. This al. Schistosomiasis, soil transmitted helminthiasis, and malaria co-
prevalence is low compared to 26.3% of 825 children that have infections among women of reproductive age in rural
shown 11. This difference could be due to different study areas, communities of Kwale County, coastal Kenya. BMC Public Health.
age-groups and sample size. 2022 Dec 1;22(1). https://doi.org/10.1186/s12889-022-12526-0
PMid:35045848 PMCid:PMC8772099

ISSN: 2250-1177 [106] CODEN (USA): JDDTAO

Jeannine et al Journal of Drug Delivery & Therapeutics. 2024; 14(5):102-107
3. Rujeni N, Morona D, Ruberanziza E, Mazigo HD. Schistosomiasis and Global Burden of Disease Study 2013. Lancet. 2015 Aug
soil-transmitted helminthiasis in Rwanda: An update on their 22;386(9995):743-800.
epidemiology and control. Vol. 6, Infectious Diseases of Poverty.
BioMed Central Ltd.; 2017. https://doi.org/10.1186/s40249-016- 11. Mazigo HD, Waihenya R, Lwambo NJ, Mnyone LL, Mahande AM,
0212-z PMid:28245883 PMCid:PMC5331630 Seni J, et al. Co-infections with Plasmodium falciparum,
Schistosoma mansoni and intestinal helminths among
4. Kinung'hi SM, Mazigo HD, Dunne DW, Kepha S, Kaatano G, schoolchildren in endemic areas of northwestern Tanzania
Kishamawe C, et al. Coinfection of intestinal schistosomiasis and [Internet]. Vol. 3, Parasites & Vectors. 2010. Available from:
malaria and association with haemoglobin levels and nutritional http://www.parasitesandvectors.com/content/3/1/44
status in school children in Mara region, Northwestern Tanzania: https://doi.org/10.1186/1756-3305-3-44 PMid:20482866
A cross-sectional exploratory study. BMC Res Notes. 2017 Nov PMCid:PMC2881914
9;10(1). https://doi.org/10.1186/s13104-017-2904-2
PMid:29121978 PMCid:PMC5679344 12. Moriyasu T, Nakamura R, Deloer S, Senba M, Kubo M, Inoue M, et
al. Schistosoma mansoni infection suppresses the growth of
5. Marcelline U, Noella U, Tharcisse M, Corine K, Josephat M, Banson B. Plasmodium yoelii parasites in the liver and reduces gametocyte
The Impact of Malaria and Gastrointestinal Helminthiasis Co- infectivity to mosquitoes. PLoS Negl Trop Dis. 2018 Jan 1;12(1).
infection on Anaemia and Severe Malaria among Children in https://doi.org/10.1371/journal.pntd.0006197 PMid:29373600
Bugesera District, Rwanda. Int J Trop Dis Heal. 2016 Jan PMCid:PMC5802944
10;13(4):1-7. https://doi.org/10.9734/IJTDH/2016/23241
PMid:26988030 13. Sturrock RF. Guidelines for the evaluation of soil-transmitted
helminthiasis and schistosomiasis at community level: A guide for
6. WHO. epidemiology of malaria worldwide. 2020. managers of control programmes. Trans R Soc Trop Med Hyg.
1998;92(4):470-1. https://doi.org/10.1016/S0035-
7. Rudasingwa G, Cho S Il. Determinants of the persistence of malaria 9203(98)91101-4
in Rwanda. Malar J. 2020 Jan 21;19(1).
https://doi.org/10.1186/s12936-020-3117-z PMid:31964371 14. Chipwaza B, Sumaye RD. High malaria parasitemia among
PMCid:PMC6975052 outpatient febrile children in low endemic area, East-Central
Tanzania in 2013. Vol. 13, BMC Research Notes. 2020.
8. RBC. Epidemiology of malaria in rwanda. 2020. https://doi.org/10.1186/s13104-020-05092-4 PMid:32448376
9. Dejon-Agobé JC, Honkpehedji YJ, Zinsou JF, Edoa JR, Adégbitè BR, PMCid:PMC7247273
Mangaboula A, et al. Epidemiology of schistosomiasis and soil- 15. Cando LFT, Perias GAS, Tantengco OAG, Dispo MD, Ceriales JA,
transmitted helminth coinfections among schoolchildren living in Girasol MJG, et al. The Global Prevalence of Schistosoma mansoni,
Lambaréné, Gabon. Am J Trop Med Hyg. 2020 Jul 1;103(1):325-33. S. japonicum, and S. haematobium in Pregnant Women: A
https://doi.org/10.4269/ajtmh.19-0835 PMid:32431272 Systematic Review and Meta-Analysis. Trop Med Infect Dis. 2022
PMCid:PMC7356410 Nov 4;7(11):354. https://doi.org/10.3390/tropicalmed7110354
10. Vos T, Barber RM, Bell B, Bertozzi-Villa A, Biryukov S, Bolliger I, et PMid:36355896 PMCid:PMC9693339
al. Global, regional, and national incidence, prevalence, and years 16. Rutagwera DG, Tylleskär T. Coinfection with Malaria, Hookworm
lived with disability for 301 acute and chronic diseases and and Schistosomiasis among School Children in Zambezi: A School-
injuries in 188 countries, 1990-2013: A systematic analysis for the based Rapid Survey 1,2 2. Vol. 39, Medical Journal of Zambia. 2012.

ISSN: 2250-1177 [107] CODEN (USA): JDDTAO