A review of soil transmitted helminthiasis in Nigeria

Abstract

Soil transmitted helminthiasis (STH) is often neglected possibly because of its low mortality
rate; however, it accounts for the highest disability adjusted life years (DALYs) among parasitic
diseases in the world. Nigeria is endemic to STH and control programmes/efforts have been
ongoing. Here, data on the burden of STH infections in Nigeria in form of years of life lost
due to mortality (YLLs), the distribution of the infection in the six geopolitical zones and the
prevalence pattern over a 37-year period are presented. The prevalence data showed reduction
in Ascaris lumbricoides and Trichuris trichiura infections; while infections with hookworm
and Strongyloides showed irregular pattern with no significant differences. Notably, YLD for A.
lumbricoides infection was the highest in the south-west; and the factors possibly impacting on
the burden of STH in Nigeria were highlighted.

Full text

841
Review article https://doi.org/10.12980/apjtd.7.2017D7-235 ©2017 by the Asian Pacific Journal of Tropical Disease. All rights reserved.
A review of soil transmitted helminthiasis in Nigeria
John Asekhaen Ohiolei1, Clement Isaac1*, Oriri Asemota Omorodion2
1Department of Zoology, Ambrose Alli University, Ekpoma, Nigeria
2Industrial Safety and Environmental Technology Department, Petroleum Training Institute, Effurun, Nigeria
Asian Pac J Trop Dis 2017; 7(12): 841-848
Asian Pacific Journal of Tropical Disease
journal homepage: http://www.apjtcm.com
*Corresponding author: Clement Isaac, Department of Zoology, Ambrose Alli
University, Ekpoma, Nigeria.
Tel: +2347058777005
E-mail: cle21200@gmail.com
The journal implements double-blind peer review practiced by specially invited
international editorial board members.
1. Introduction
Soil transmitted helminthiasis (STH) are parasitic infection caused
mainly by Ascaris lumbricoides (common roundworms), Trichuris
trichiura (whipworms), and the hookworms Necator americanus
and Ancylostoma duodenale. Of the 1.5 billion infected, about 270
million and 600 million are preschool and school-aged children,
respectively. Conditions relating to the epidemiology of STH are
mostly linked to poverty as sufferers are mainly from the world’s
most impoverished regions[1]. The Americas, China, East Asia and
sub-Saharan Africa account for over 56% of the STH infection
globally[2].
The developmental stages of the nematodes causing STH are
partly in the soil and in vertebrate host(s). In worse case scenarios,
STH may impact on the mental health of children as well as bring
about malnutrition leading to growth retardation[3,4]. Among
neglected tropical diseases, STH accounts for the highest disability
adjusted life years (DALYs), which include years of life lost due
to mortality (YLLs) and years lived with disability (YLDs)[5].
Despite having the highest DALYs of approximately 5.2 million
in comparison to schistosomiasis (3.3 million DALYs), lymphatic
filariasis (2.8 million DALYs) and onchocerciasis (0.5 million
DALYs)[5], STH receives relatively less attention in aspects of
monitoring and treatment[6].
In Nigeria, the need to appraise prevalence data overtime is now
imperative as this would inform on the possible gains/losses that
have been made. Further, the challenges of current diagnostic
methods used in the country with the problem of drug resistance in
achieving the elimination goal are thus highlighted.
2. Methodology
Literature search was done on Google Scholar and PubMed
databases using relevant keywords. Studies on the prevalence of
STH (Ascaris, hookworm, Trichuris and Strongyloides) in Nigeria
were selected and reviewed. Prevalence data from the surveyed
States categorised under the six geopolitical zones were analysed.
ARTICLE INFO ABSTRACT
Soil transmitted helminthiasis (STH) is often neglected possibly because of its low mortality
rate; however, it accounts for the highest disability adjusted life years (DALYs) among parasitic
diseases in the world. Nigeria is endemic to STH and control programmes/efforts have been
ongoing. Here, data on the burden of STH infections in Nigeria in form of years of life lost
due to mortality (YLLs), the distribution of the infection in the six geopolitical zones and the
prevalence pattern over a 37-year period are presented. The prevalence data showed reduction
in Ascaris lumbricoides and Trichuris trichiura infections; while infections with hookworm
and Strongyloides showed irregular pattern with no significant differences. Notably, YLD for A.
lumbricoides infection was the highest in the south-west; and the factors possibly impacting on
the burden of STH in Nigeria were highlighted.
Article history:
Received 19 Oct 2017
Received in revised form 30 Oct 2017
Accepted 18 Nov 2017
Available online 29 Nov 2017
Keywords:
Soil transmitted helminthiasis
DALYs
YLD
Nigeria

John Asekhaen Ohiolei et al./Asian Pac J Trop Dis 2017; 7(12): 841-848
842
Rural to urban ratio, STH prevalence and YLD were estimated.
Statistical analyses using One-way ANOVA were applied with
GraphPad Prism version 5.01 (GraphPad software, San Diego, CA,
USA). Mean differences are significant at P < 0.005.
3. Study on STH infection in Nigeria: the limitation
STH investigation in Nigeria spans over nine decades[7].
Historically till date, there are little or no changes regarding the
tools/methods used for STH study as microscopy remains in-
use. In some cases, geographic information systems have been
applied in order to gather supporting data for risk mapping and
predictive studies[8]. However, molecular techniques in relation
to identification and prevalence studies of species of STH are
yet to be applied in epidemiological surveys in Nigeria. This is
due to its relatively high cost and the requirement of specially
trained technical staff. The molecular technique is now becoming
an unavoidable method because it is capable of overcoming the
challenges of misidentification as it is highly sensitive and specific.
A case in point is the difficulty in differentiating hookworm species
for which data in Nigeria are largely speculative. In addition,
the possibility of other Trichuris species to be responsible for
trichuriasis is considerably high but has not been investigated using
more species-specific methods. Meanwhile, elsewhere, there is
the growing use of molecular techniques[9], and recently, Necator
americanus was the dominant hookworm species among children[9].
Similarly, a relatively high prevalence of STH across some endemic
countries was confirmed by using PCR-restriction fragment length
polymorphisms and Trichuris vulpi was identified in some of the
children[10]. The prospect and potential of PCR-based detection
methods using next-generation sequencing approach is seriously
gaining attention globally[11,12].
4. Prevalence and distribution of STH infection
In Nigeria, STH studies have been focused mostly on children (pre-
school and school-age) (69%) than adults (31%); and mostly in rural
(68.9%) than urban areas (31.1%) (Figure 1). Age group of 4–10
years is the high risk group and most infected[13-15]. Children within
this age group are highly active with frequent soil contact during
play hours both at home and in school. Infection in relation to sex is
often linked to external/environmental factors with males indulging
more in risk behaviour than their female counterparts[16,17].
Survey data (1980 to early 2017) from the six geopolitical zones
showed a decreasing trend in prevalence for A. lumbricoides (F =
3.89; P = 0.012) and T. trichiura (F = 3.44; P = 0.021) (Figure 2).
Meanwhile, hookworm (F = 1.506; P = 0.220) and Strongyloides
(F = 0.705; P = 0.555) showed irregular prevalence pattern. Drugs
against hookworm are most times ineffective because of the drug
resistance[18-20].
60
50
40
30
20
10
0
Mean prevalence (%)
Ascaris Hookworm Trichuris Strongyloides
Rural Urban
STH
Figure 1. Urban-rural prevalence of STH infection.
70.0
60.0
50.0
40.0
30.0
20.0
10.0
0.0
1980-1990 1991-2000 2001-2010 2011-2017
Ascaris Hookworm Trichuris Strongyloides
Figure 2. Mean prevalence of STH in the last four decades (1980–2017).
Across the geopolitical zones of the country, STH burden was
the highest in the southern region (south-west, south-east, and
south-south) compared to the northern region (Table 1). This could
be attributed partly to the climatic conditions in the south where
helminths thrive more in these conditions than in dry and arid
conditions in the north. STH prevalence for the north-eastern region,
however, could not be estimated due to limited available data.
Table 1
Mean prevalence and estimated YLD according to geopolitical zones (2005–2017).
Region Ascaris Hookworm Trichuris Strongyloides
Mean ± SD (%) YLD per 10 000 Mean ± SD (%) YLD per 10 000 Mean ± SD (%) YLD per 10 000 Mean ± SD (%) YLD per 10 000
South-west 31.9 ± 18.6 86.0 12.0 ± 13.5 32.5 8.5 ± 9.6 23.0 8.8 ± 10.1 23.8
South-south 23.7 ± 19.9 63.9 12.4 ± 10.2 33.4 8.5 ± 11.9 23.1 1.2 ± 0.5 3.0
South-east 18.1 ± 14.1 48.9 23.4 ± 26.9 63.3 7.0 ± 6.0 19.0 3.7 ± 4.9 10.0
North-central 6.6 ± 4.5 17.7 14.9 ± 12.6 40.2 6.3 ± 2.8 17.0 6.7 ± 8.4 18.2
North-west 9.1 ± 7.5 24.6 9.1 ± 8.5 24.7 3.2 ± 4.6 8.6 7.9 ± 10.9 21.3
North-east N/A N/A N/A N/A N/A N/A N/A N/A
N/A: Not available.

John Asekhaen Ohiolei et al./Asian Pac J Trop Dis 2017; 7(12): 841-848 843
5. Risk factors
Environmental factors and conditions influencing STH transmission
are similar to those existing elsewhere in the tropics and other sub-
Saharan African countries. Meanwhile, habits known to impact
on STH infection and prevalence include open bush defecation[21-
23], walking barefooted, geophagy and onychophagy[21,24]. Other
risk factors have been linked to occupation of parents, sources of
drinking water and poor personal hygiene[21,22,25-30]. The role of
the soil as reservoir in maintaining the transmission cycle cannot be
overstated[31].
The burden of infection in relation to the immune status of
individuals has demonstrated higher prevalence among HIV positives
than HIV negatives. Prevalence of STH in HIV sero-positive group
could be twice the prevalence in HIV sero-negative group[32-35].
6. DALYs and infection burden
DALYs have become a fast growing metric measurement to
assessing disease burden[36]. A lot of reports on STH from Nigeria
have been documented, especially from rural communities and in
children but reports of infection burden measured in DALYs are
unavailable. Here we provide an estimated value of YLD based on
available prevalence data and morbidity of infection[37].
YLD due to STH in this review was estimated using the formula
below[38]:
YLD = P × DW
where, P = number of prevalent cases, DW = disability weight.
Here, prevalence was used rather than incidence[38] because in
Nigeria, surveys are widely reported in prevalence (Table 2). DW
(0.027) of intestinal helminth infection which is represented on a
Table 2
Epidemiological survey (prevalence) of STH in Nigeria (1977–2017).
State No.
Sampled
Ascaris
(%)
Hookworm
(%)
Trichuris
(%)
Strongyloides
(%)
Study population Ref
Abia 338 36.60 26.00 13.00 - Primary school children [39]
Akwa Ibom 316 18.00 21.50 13.30 2.80 Primary school pupils [40]
Akwa Ibom 405 24.20 41.70 4.70 - School-aged children [41]
Anambra 1536 20.80 13.00 15.30 1.30 School-aged children [42]
Bauchi 1037 22.50 4.40 1.50 - Rural dwellers [43]
Benue 418 - 35.40 3.80 - Pre-school children [44]
Benue 580 11.89 18.62 4.65 1.89 Primary school children [45]
Borno 257 19.10 N/A 3.50 N/A Almajiris [46]
Cross River 350 64.40 10.90 1.10 - Preschool children [47]
Delta 194 42.78 28.35 11.34 1 School-age children [48]
Delta 1351 48.41 29.76 17.39 - School-age children [49]
Delta 211 45.97 13.27 20.38 School children [50]
Ebonyi 576 10.90 7.50 4.20 - School-aged children [51]
Ebonyi 510 10.80 4.30 1.20 0.60 Primary school children [52]
Edo 1166 10.80 9.20 1.70 - Rural dwellers [53]
Edo 200 4.00 15.00 0.50 1.00 Primary school children [54]
Edo 192 25.00 13.02 - 1.00 School-age children [48]
Edo 3601 6.50 2.80 1.40 - Randomly selected individuals from the state [55]
Edo 6213 19.50 16.90 5.90 - Hospital patients [56]
Edo 207 11.10 5.80 3.80 0.50 Outpatient children [57]
Edo 2000 6.00 3.70 0.90 1.20 HIV infected individuals [32]
Edo 500 4.20 1.40 - - HIV control individuals [32]
Edo 496 6.90 2.40 0.20 - Out-patient children [30]
Edo 862 38.20 29.40 27.30 - Individual from 3 geographic zones of the Defunct Bendel State [58]
Edo 140 18.60 - 2.10 - Children from orphanages [59]
Enugu 6842 20.60 71.10 7.90 0.40 Rural dwellers [60]
Enugu 407 22.90 32.40 2.50 1.00 School children [13]
Enugu 1296 4.90 2.50 0.70 - School children [23]
Enugu 255 46.00 23.00 9.00 11.00 Primary school children [14]
Enugu 1269 Children and adults [61]
Enugu 242 12.40 29.30 16.50 0.40 Primary school pupils [62]
Enugu 13385 7.40 14.30 2.20 0.90 Outpatients individuals [63]
Enugu 1296 4.90 2.50 0.70 School children [64]
Imo 284 2.30 94.20 - - Primary school pupils [65]
Imo 96 28.10 5.20 - - School-aged children [66]
Imo, Abia, Enugu and Ebonyi 231 2.60 3.90 - 1.70 Nomads [67]
Kano 570 7.90 5.30 3.50 - Apparently healthy children [68]
Kano 105 - 3.80 - - HIV infected individuals [34]
Kebbi 1357 9.95 13.63 0.29 - Inhabitants of Bagudo, Dandi and Zuru L.G.A [69]
Kwara 90 6.70 7.80 10.00 18.90 HIV positive individuals [33]
Kwara 90 6.70 7.80 6.70 5.60 HIV negative individual [33]
continued on next page

John Asekhaen Ohiolei et al./Asian Pac J Trop Dis 2017; 7(12): 841-848
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scale of 0–1 (0 = perfect health; 1 = death), was adopted[104]. YLDs
due to STH according to the geopolitical zones are shown in Table 1.
7. Control efforts
The achievement of control and elimination relies largely on
chemotherapy through mass drug administration (MDA). Drugs
commonly administered against STH in Nigeria are albendazole,
pyrantel and levamisole. These drugs have demonstrated varying egg
reduction and curative rates (Table 3). There are increasing reports
of mass deworming programme across the country[69,109,110], and
studies have suggested that sustainable decrease in infection burden
is a result of continuous use of antihelminthics[69,78].
The previously high and recently decreased rate of infection in
communities may be due to MDA, increased community awareness
and other control efforts[78]. Other practices largely responsible
for decreasing STH prevalence across the country include growing
educational and socio-economic status of parents/caregivers[25,26,30]
with an increasing percentage of children now using foot wears both
at home and in school[26]. Clearly, integrated control methods have
been responsible for the observed trend in STH prevalence[111].
8. Conclusion
This review presents the limitations of the present tools used for
STH investigation in Nigeria, and highlights the need to apply a more
sensitive and specific diagnostic tool in epidemiological studies.
Meanwhile, the mean prevalence of the pooled survey data over four
Table 2 (continued)
State No.
sampled
Ascaris Hookworm Trichuris Strongyloides Study population Ref
Kwara 907 40.90 10.20 27.00 9.70 Children [70]
Lagos 300 67.70 45.00 31.30 18.00 Rural dwellers (aged 1–80) [71]
Lagos 1177 29.70 0.70 18.40 0.30 Randomly selected children [72]
Lagos 5595 74.20 29.50 75.80 - Primary school children [73]
Ogun 218 9.60 4.13 1.84 - Rural dwellers [26]
Ogun 232 31.90 3.50 16.40 - School children [25]
Ogun 1059 53.40 17.80 10.40 0.70 School children [27]
Ogun 479 40.00 19.20 23.20 2.10 Urban dwellers [74]
Ondo 180 22.20 10.60 - 12.80 Primary school pupils [75]
Ondo 1076 75.30 7.60 84.00 - School children in riverine community [3]
Osun 766 88.50 33.10 84.50 3.00 Primary school children [76]
Osun 312 39.10 - - - School children [77]
Osun 625 47.60 4.30 3.70 - School-aged children [78]
Osun 162 36.40 5.60 - 3.70 Primary school [79]
Osun 283 39.90 18.40 21.90 - Individuals from Iwo LGA [80]
Osun 369 12.20 - 1.40 - 0–25 months [81]
Osun 395 44.80 19.50 14.00 - Primary school [15]
Osun 300 4.30 0.30 1.30 - Diarrheic children [82]
Osun 200 35.00 17.50 - 0.50 Children in secondary health care facility [83]
Osun 52 1.90 - - - HIV infected children [35]
Osun 309 67.00 43.70 20.70 25.60 School-aged children [84]
Osun 465 30.10 4.90 0.60 Malnourished school children [85]
Osun 284 23.20 3.90 0.40 Well-nourished school children [85]
Osun 250 14.80 9.20 2.00 Primary school pupils [86]
Oyo 1434 61.5–72.2 52.4–63 65–74 - Rural dwellers [87]
Oyo 470 49.40 14.80 15.80 - Rural dwellers [88]
Oyo 248 40.70 4.40 4.80 - School-aged children [89]
Oyo 957 25.80 9.30 0.60 - School-aged children [90]
Oyo 478 70.00 46.00 4.00 - N/A [91]
Oyo 1273 39.00 26.50 28.40 - Urban children [92]
Plateau 300 0.70 17.00 1.70 0.23 Rural dwellers [93]
Plateau 1080 84.70 91.90 74.20 50.30 Dry season farmers [94]
Plateau 204 0.98 4.90 - 0.50 Rural and urban dwellers [95]
Rivers 396 11.00 36.00 4.00 - Rural dwellers [96]
Rivers 5451 49.30 31.40 40.70 - Rural dwellers [97]
Rivers 280 18.20 5.40 3.50 3.50 Rural dwellers [98]
Rivers 2008 24.10 18.00 17.30 10.10 Rural dwellers [99]
Rivers 3826 14.30 6.90 4.20 2.00 School children [100]
Rivers 300 54.00 42.70 43.70 33.00 Urban and suburban dwellers [101]
Rivers 215 33.30 27.30 39.40 - School children [16]
Rivers 1062 51.90 1.00 41.70 1.40 Preschool children [102]
Sokoto 1620 0.10 1.00 0.10 0.20 Infants (1–24 months) [103]
Zamfara 519 18.50 22.00 8.80 15.60 Nomadic fulanis [22]
N/A: Not available.

John Asekhaen Ohiolei et al./Asian Pac J Trop Dis 2017; 7(12): 841-848 845
decades across the country shows a decreasing trend for Ascaris
and Trichuris infection. However, the need to regularly update the
national prevalence and DALYs would be helpful in tracking the
progress of control efforts. In addition, the government has to live
up to its responsibility by ensuring it abides by the recommendation
of the World Health Assembly of 100% target-treatment of school-
age children annually in places with > 50% STH prevalence. It is
also imperative to engage research in determining the level of drug
resistance with the view to applying the most effective chemotherapy
regimen. Ultimately, an approach for elimination is to identify risk
factors peculiar to different communities/regions in Nigeria.
Conflict of interest statement
We declare that we have no conflict of interest.
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Osun Albendazole (200–400 mg) 625 89 33 1–4 [78]
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Ebonyi Albendazole 576 100 > 90.6 6–17 [51]
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