Community Wide Cross Sectional Survey
Community Wide Cross Sectional Survey
Research Article
Long Term School Based Deworming against Soil-Transmitted
Helminths Also Benefits the Untreated Adult Population:
Results from a Community-Wide Cross Sectional Survey
Received 17 January 2019; Revised 8 March 2019; Accepted 17 March 2019; Published 2 May 2019
Copyright © 2019 Paul M. Gichuki et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Background. Soil-transmitted helminths (STH) are a public health problem in Kenya. The primary control strategy for these
infections is preventive chemotherapy (PC) delivered through school based deworming (SBD) programs. The World Health
Organization (WHO) recommends the inclusion of other at-risk groups in the PC. The untreated groups in endemic areas have
been shown to act as reservoirs for STH transmission. Few field based studies have focused on the possible benefits of SBD to the
untreated groups in the community. This study sought to determine the levels of STH among all age groups in a community where
SBD has been going on for more than 10 years. Methods. This was a cross sectional study where 3,292 individuals, ranging from
2 to 98 years, were enrolled. Stool samples were analyzed using duplicate Kato Katz thick smear technique for presence of STH
eggs. Statistical analysis was conducted using STATA software 14.0 (Stata corporation). Results. Out of the total 3,292 stool samples
analyzed, only 13 were positive for any STH. Of these, 12 were infected with Trichuris trichiura and one case was of hookworm.
There was no Ascaris lumbricoides infection detected. Of the 13 STH infections, seven of the infections were of school going age
(6-18 years), 5 were of preschool age (<6 years), and one was of adult age group (18>). More male (61.5%) than female were infected
with STH. Conclusion. This study shows very low prevalence of STH among all age groups in Mwea, suggesting that long term SBD
may also be benefitting the untreated groups in the community and thus the potential to achieve STH elimination in such endemic
areas.
(dose of 400 mg) and mebendazole (dose of 500 mg), which After the initial mass deworming, a cohort of 2300
are widely used in programs, levamisole (dose of 2.5 mg children aged between 4 and 18 years from 5 sentinel schools
kg−1 ), and pyrantel pamoate (dose of 10mg kg−1 ) which is less were followed up at multiple points each year for four years
commonly used [9, 10]. and examined for intestinal helminths. The result of the above
The WHO goal to scale up chemotherapy for STH was study indicates that at baseline, the prevalence of any STH
endorsed in the London declaration of 2012, so that by 2020, was 19.2 % (95% CI 0.5-1.2%). Hookworm was at 16.7% (95%
75% of the preschool and school going children in need will CI 15.2-18.2%), Ascaris lumbricoides was at 1.7% (95% CI
be treated regularly [1]. Recent WHO data shows that by 1.1-2.2%), and Trichuris trichiura was at 0.8% (95% CI 0.5-
the year 2017, 743 million people had received preventive 1.2%). The mean intensity as measured by eggs (per gram of
chemotherapy for STH (188 million preschool-aged children, faeces 9 epg) was at 1.647 for hookworm, 0.245 for Ascaris
410.1 million school-aged children, and 127.9 million women lumbricoides, and 0.053 for Trichuris trichiura. Among the
of reproductive age). [11]. These are the three priority groups 4 age groups analyzed in the study (3-5, 6-10, 11-15, and 16-
identified by WHO for deworming through mass drug 18 years old) prevalence of hookworm was highest among
administration [12]. However in Kenya, only school going the 16-19-year-old and decreased steadily to the 3-5-year-old
children are targeted in the SBD program [13] as they typically patients [21].
harbor chronic and intense infections at a time when they are Other studies previously carried out in the area have
undergoing physical and/or cognitive development [12, 14] reported soil eating, hand washing, and shoe wearing as risk
and the relative ease of access to children in rural areas factors for STH infection [27]. Sanitation coverage among
through schools [15]. households in the area has been reported at 73% [28]. In the
schools, a study reported that more than 50% of toilets were in
However, reinfection after chemotherapy has been shown
poor hygienic conditions [29]. The study further notes that as
to commonly occur [16, 17]. This has been largely attributed to
at the year 2014, not much had changed in regard to sanitation
the subgroups in the larger community who usually are not
facilities in the schools [29].
covered in the SBD, including the preschool going children
Adult age groups who do not have access to STH
and the adult community [18]. These groups of people
treatment have been shown to benefit from the school
although untreated sometimes have disproportionately heavy
based deworming as a result of its impact on the overall
burden of infection [19]. Another factor is the ability of the
transmission intensity within that population [30]. Treatment
helminth eggs and larvae to survive for extended periods in
of preschool and school age children reduces the output of
the environment thus creating a source for rapid reinfection
infective stages in faeces that result in the contamination
following chemotherapy [20]. Thus long term effectiveness
of the environment in which everybody else lives [31].
of school based deworming in interrupting STH infection is
Surveillances which are school based have been shown to
dependent on maintenance of regular treatment [19].
give good estimates of the reduced morbidity in children
In Mwea, Kirinyaga County, Central Kenya, annual SBD but can lead to misleading estimates of the impact of these
with albendazole covering all the primary schools in the area programs on overall transmission in the community [32].
has been going on since the year 2004 [21]. The deworming Most of the studies that have been carried out in this area
programme was initiated through collaboration between have focused on school going children [24, 33]. Very few
Japan International Corporation Agency (JICA) and Kenya field based studies have focused on the possible effect of the
Medical Research Institute (KEMRI), Eastern and Southern ongoing school based deworming programs on the larger
Africa Center of International Parasite Control (ESACI- community. Much of this information comes from mathe-
PAC), and involves annual mass drug administration of matical modeling studies, whose findings do not anticipate
antihelmintics to all school-aged children [21]. The treatment an impact of the SBD on the larger community [24]. Field
includes a single dose of 40 mg/kg of praziquantel using the based epidemiological data on community-wide prevalence
tablet dose pole to determine the number of tablets [22, 23] and intensity of STH especially in areas where school based
and albendazole in a 400mg single dose. The deworming deworming is ongoing is important so as to inform decision-
program temporally stopped for two years (2010 and 2011) making on the feasibility of including the larger community
and resumed in the year 2012 under the Kenya National in the SBD programs, and also the potential benefits of the
school based deworming programme. SBD to the untreated groups. The current study sought to
Before the start of the above program in the year 2004, a determine the prevalence of STH among all age groups in a
baseline parasitological survey on STH and schistosomiasis community where SBD has been going on for more than 10
was conducted in a total of 86 schools in Mwea. All children years.
in these schools were then treated annually with albendazole
(400mg) and praziquantel [21]. Treatment coverage between 2. Materials and Methods
the years 2004 and 2009 was reported at approximately
40,000 school going children [24]. During the years 2012- 2.1. Study Area and Population. The study was conducted
2013, treatment coverage for Mwea was 48,602 [25], while in Mwea East and West Subcounties of Kirinyaga County,
in 2013-2014, the coverage was at 46,999 [26]. The annual Central Kenya. It is located about 100kms north east of
treatment of the school going children has continued in all Nairobi and has two rainy seasons, the long rains and the
the schools in the area over the years, except for year 2010 short rains. It has an estimated 154,220 households and a
and 2011 when the program stopped temporally. total population of 528,054 persons, with an annual growth
Journal of Tropical Medicine 3
rate of 1.5 percent. The population was projected to be 595, provided with a clean, dry, and leak proof stool container
379 in 2017. The majority of the population are of Kikuyu labeled with a unique identifier and asked to provide a stool
tribe [34]. Mwea East and West Subcounties are home to the sample. The samples were then collected in a cooler box and
giant Mwea irrigation scheme. Rice and horticultural farming transported to the laboratory for examination. Screening of
are the main socioeconomic activities in the area. Several STH eggs was based on duplicate Kato-Katz thick smears of
water channels crisscross the area supplying irrigation water 41.7 mg prepared from fresh stool samples to determine the
to the farms and villages, respectively. STH was previously prevalence and intensity of STH [36]. For quality assurance,
determined to be endemic in this area [21, 24]. a random sample of 10% of all the positive and negative slides
read each day was randomly reexamined by third experienced
2.2. Study Design and Sample Size. This was a cross sectional laboratory technologists.
study carried out between the months of August and October
2017. A minimum sample size of 905 households was cal- 2.5. Ethical Considerations. The study was reviewed and
culated using the formulae by Fishers et al [35]. From each approved by the Scientific and Ethical Review Unit (SERU)
household sampled, all members of the household present of the Kenya Medical Research Institute (KEMRI), number
were asked to provide a stool sample. (KEMRI/SERU/ESACIPAC/007/ 3326), and Meru University
of Science and Technology Institutional Research Ethics
2.3. Study Population and Selection Criteria. Multistage sam- Review Committee (MIRERC), number MIRERC/001/2017.
pling was used where two locations from each of the two sub- The study received further clearance from Kirinyaga County
counties were randomly selected. Mwea East Subcounty had a Health team. A written informed consent (Swahili translated)
total of five locations including Murinduko, Tebere, Nyangati, to participate in the study was obtained from all the adults
Kangai, and Gathigiriri while Mwea West Subcounty had and an assent sought from all participating children before
three locations Wamumu, Thiba, and Mutithi. Using simple conducting an interview or collecting a stool sample. For
random sampling, one location from each of the two sub- illiterate individuals, a thumb print was used to sign the
counties was selected to participate in the study. Thus, Tebere assent and consent forms after a clear description of the study
and Thiba locations from Mwea East and West Subcounties, objectives and acceptance to participate.
respectively, were selected.
From the locations selected, a list of all villages in each 2.6. Data Management and Analysis. Data collected was
location was obtained. Thiba location had a total of eight vil- entered and stored in an excel spreadsheet. It was then
lages including Mbui Njeru, Maendeleo, Gakungu, Rurumi, counter-checked for accuracy. Statistical analyses were car-
Thiba, Karima, Kiratina, and Kasarani, while Tebere loca- ried out using STATA version 14.0 (Stata Corporation, Col-
tion had six villages which included Kamucege, Gathigiriri, lege Station, TX, USA). Infection with STH was defined
Block, Kiarukungu, Mahigaini, and Kirogo. Using random based on the presence of an egg across the duplicate slide
sampling, four villages were selected in Thiba location which readings while intensity was expressed as the arithmetic
included Karima, Kasarani, Gakungu, and Rurumi, and three mean of eggs per gram (epg) of faeces across the two slides.
villages in Tebere location including Kirogo, Kamucege, and The prevalence of STH was calculated as percentage of the
Block villages. positive participants. The 95% confidence intervals (95% CI)
The study then used probability proportional to size sam- were calculated using binomial logistic regression. Infection
pling to determine the minimum number of households to be intensities were classified into light, moderate, and heavy
sampled per village. Each study village was mapped, whereby infections, according to WHO guidelines [37].
all the households in each village were recorded. Systematic
sampling was then used to select households within each 3. Results
village. The first household was randomly selected at the
center of the village and, thereafter, every third household The study enrolled a total of 905 households in seven villages.
from each direction of the first household was surveyed. From the selected households, a total of 3,292 individual
Household heads or their representatives from the sampled members gave a stool sample. Each household had an average
households in each village were interviewed. Sensitization of four members. The mean age was 27 years (standard
meetings were held in all the villages with the community deviation ± 18 years) with an age range of 2 to 98. Out of the
members, community leadership, and the local administra- total participants, 255 (7.8%) were of preschool going age, 1,101
tion to explain to them the study and seek their consent. (33.5%) of school age, and the rest 1.936 (58.8%) of adult age
In each of the sampled households, all individuals present group. Over half of the study participants 1770 (53.8%) were
at the time of survey from age 2 years were asked to provide female (Table 1).
a stool sample after consenting and assenting for the younger
children. A written informed consent was further obtained 3.1. Prevalence of STH and Other Helminths among the Study
from each participating household head prior to the survey. Participants. Of the 3,292 stool samples analysed in this
study, only 13 of them tested positive for any STH. Of the
2.4. Stool Sample Collection and Laboratory Analysis. In 13 samples that tested positive for STH infection, 12 had
each household, data on selected demographic characteristics Trichuris trichiura and one had hookworm infection. There
like age and gender of every participant who consented to was no sample that tested positive for Ascaris lumbricoides. Of
provide a stool sample were recorded, and the person was the 13 STH infections, five were of preschool age (>6 years),
4 Journal of Tropical Medicine
Table 1: Demographic characteristics of the study participants. of 60 (24 - 156) epg. Majority of the S. mansoni infections
(65.3%) were of light intensity (1-99 epg).
Characteristic Frequency (n=3292) Percentage (%)
Age (Years)
4. Discussion
<6 255 7.8
6-18 1,101 33.5 The main goal of STH control programs, which typically
>18 1,936 58.8 involves preventive chemotherapy, delivered through schools
Gender [12], is to reduce the prevalence of moderate to heavy
Male 1522 46.2 intensity of infections of any STH to below 1% of the at-risk
population [38]. Other than the school going children, WHO
Female 1770 53.8
recommends that other at-risk populations in the community
Village be included in the preventive chemotherapy. In Kenya the
Gakungu 431 13.1 control strategy largely is through school based deworming
Kamucege 532 16.2 programme, which was launched in the year 2009 with an aim
Karima 391 11.8 of reducing the prevalence of STH in school age children to
Kasarani 454 13.7 below 4% [39, 40].
Kirogo 381 11.8 The current findings show very low infection with STH
Rurumi 737 22.3
among all age groups, including preschool (<6 years) and
school-aged children (6-18 years) as well as the adult pop-
Block 366 11.1
ulation (>18 years) in an area that has been endemic for
these infections. These results support previous findings
which have reported low prevalence of STH among preschool
seven cases were of school going age (6-18 years), and one children [27] and school age children [33]. In the more than
was an adult. The single case of hookworm was a male adult 10 years through which the SBD programme has happened
of 20 years. Male participants were more infected with STH in the study area, the adult community have not received
(61.5%) than female. Other helminths detected in the study treatment, yet only one adult was found to be infected
included S. mansoni 20.1% (95% CI 18.8-21.5%), Hymenolepis with hookworm. This supports previous studies which have
nana 0.9% (95% CI 0.6 – 1.3%), and one case of Taenia species reported that treating school children through SBD may also
(Table 2). Analysis of the stool samples also revealed that 672 benefit the adult age groups even when they do not receive
participants were infected with either species of STH or S. treatment [30]. Previous modeling studies have suggested
mansoni or both (prevalence: 20.4%, (95% CI: 19.1%- 21.8%). that school-aged deworming may confer little benefits outside
the children being dewormed and that intensifying either
treatment coverage or increasing the frequency of treatment
3.2. Household Level Prevalence of STH. Analysis of infec- may not have an impact on the larger community [31].
tions at household level is shown in Table 3. Of the 905 The baseline results at the beginning of the SBD pro-
households whose members were enrolled in the study, 9 gramme in Mwea showed that the highest burden of STH
households had at least one member who was positive for was hookworm which was highest among the almost adult
STH. Another 431 households had at least one member who age group 16-19 years, where in some schools the prevalence
was positive for either STH or S. mansoni or both (prevalence: was as high as 28.5%. The prevalence of Ascaris lumbricoides
47.6%; 95% CI: 44.4% - 50.9%). The proportion of households and Trichuris trichiura was low in all the age groups [21].
which had at least one member testing positive for S. mansoni In the current study, only one hookworm infection was
was 47.0% (43.7% - 50.2%). The household level prevalence reported. These results suggest that sustained SBD for a
of H. nana was 3.1% (95% CI 2.2% - 4.4%). Hookworm and longer period may actually have an impact on the larger
T. trichiura infections were reported in, respectively, one and community, especially for hookworm species. However, in
eight of the nine households whose members were positive countries where resources are scarce, sustaining SBD for a
for STH. A. lumbricoides were not detected in the stool longer period may not be a viable option as it is costly
specimens observed in this study. and many of such programs are usually donor funded.
Therefore incorporating other control strategies to the SBD
3.3. Intensities of Infections. The intensities of intestinal par- programs such as improvement in the sanitation conditions
asites’ infections are displayed in Table 4. The twelve cases of both in schools and at home may help countries achieve STH
T. trichiura infections recorded were of light intensity (1-999 elimination much sooner.
epg). The number of eggs observed for T. trichiura ranged Treating school going children basically reduces the rate
from 12 to 72 eggs per gram. The range for the number of eggs at which infective stages of the STH are released to the envi-
detected in samples that were positive for infection with H. ronment. When this is sustained over a period of time, the
nana was 408 – 15480 epg while the median (IQR) egg counts entire community may indirectly benefit from the treatment
was 3,468 (606 – 12,240) epg of faeces. Hook worm had low even when they are not treated as there will be reduced
intensity infection of 24 epg. The number of S. mansoni eggs exposure to infective eggs and larvae in the environment
observed in the specimens ranged from 12 to 5,244 eggs per [30, 41]. Indeed, studies have shown that treating a few
gram (epg) of faeces with a median interquartile range (IQR) individuals in the community can impact on the effective
Journal of Tropical Medicine 5
Table 2: Prevalence of STH and other helminths among the study participants.
Species Number %
STH
T. trichiura (n=12)
Range (Min -max) 12 - 72
Median (Interquartile range (IQR)) 12 (12 – 12)
Light (1-999 epg) 12 100.0
Moderate (1,000 - 9,999 epg) 0 0.0
Heavy (≥10,000 epg) 0 0.0
Other Helminths
S. mansoni (n=663)
Range (Min -max) 12 - 5244
Median (Interquartile range (IQR)) 60 (24 - 156)
Light (1-99 epg) 433 65.3
Moderate (100 - 399 epg) 150 22.6
Heavy (≥400 epg) 80 12.1
H. nana (n=29)
Range (Min -max) 408 - 15480
Median (Interquartile range (IQR)) 12240 (606 - 3468)
reproductive number of the parasites and therefore reduced diagnostic techniques which are more robust and whose
exposure to infective stages in those untreated [31]. STH sensitivity is not affected by reduction in worm loads. Kato
parasites reproduce sexually within the human host; thus, Katz technique, recommended by WHO for quantification
both sexes need to be present within a single host for them of STH eggs in stool [37] is the most common technique
to produce fertilized eggs [42] which are expelled to the used in field surveys. It is a relatively cheap technique that
environment. Treating school age children over a long period is easy to apply in resource poor settings [44]. However, its
of time reduces the chances of both sexes of STH residing in sensitivity has been shown to reduce with the reduction of
a single human host thus limiting their sexual reproduction. STH prevalence [45, 46], making it unsuitable in low STH
This may explain the low prevalence recorded in the present intensity settings. Use of this technique in our study is a
study after a long period of SBD. In the study area, SBD has potential limitation owing to the low prevalence of STH
been ongoing since the year 2004 [24, 39, 40], with a two- reported.
year lapse (2010 and 2011) and then uninterrupted since 2012 The FLOTAC technique has been shown to have high
to date. sensitivity even in low intensity settings [45, 47]. It however
These findings also point to a possibility of the study area requires a centrifuge and longer sample preparation time
reaching a breaking point for all the STH if SBD is sustained. [48]. Future STH evaluations in this area should endeavor
Breaking point typically occurs at levels of below one parasite to collect multiple consecutive samples to cater for the daily
owing to the aggregated distribution of worm numbers per variations of egg excretion and the nonequal distribution of
host [8]. This therefore calls for frequent monitoring and eggs in a stool sample, which leads to varying egg counts
evaluation of the impact of SBD which are not only school between stool samples from the same person [49], and
based but which involves the entire community. Sustained consider use of the FLOTAC technique for stool diagno-
prevalence and intensity evaluations in this setting will even- sis.
tually provide useful practical, field based data on how long
SBD should be administered to school children for eventual 5. Conclusion
interruption of STH in the whole community. Currently,
this information has been provided through mathematical This study shows low prevalence of STH among all age groups
models [8]. including the preschool, school going, and the adult in the
Recent studies have suggested the need to shift from community, suggesting that long term SBD may also be
morbidity control to interruption of transmission for STH benefitting the untreated groups and thus the potential to
[7, 32], noting that in areas of low transmission, treating achieve STH elimination in the area. This study recommends
school children alone over a long period of time could that SBD is continued among school going children so
actually interrupt transmission [43]. Such a shift will require as to sustain the low worm load and probably eventual
availability of prevalence and intensity data for all age groups elimination of STH. The study further recommends that
and not only the school going children. As the worm burden future surveillances should not only be focused on the school
reduces to such low levels, future surveys need to use age children but also include the larger community.
Journal of Tropical Medicine 7
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Authors’ Contributions transmitted helminth infections: systematic review and meta-
analysis,” Journal of the American Medical Association, vol. 299,
Paul M. Gichuki and Charles Mwandawiro conceived and no. 16, pp. 1937–1948, 2008.
designed the study. Paul M. Gichuki and Tabitha Kimani were [11] WHO 2017, “Schistosomiasis and soil transmitted helminthi-
involved in field data collection, analysis, and manuscript ases: numbers of people treated in 2017,” Weekly Epidemiological
preparation. Edwin Kiplelgo and Paul M. Gichuki were Record, vol. 93, pp. 681–692, 2018.
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