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ORIGINAL ARTICLE
Year : 2021  |  Volume : 10  |  Issue : 1  |  Page : 65-69

Onchocerca volvulus infection among ivermectin-treated population in a rural setting in Edo State, Nigeria


1 Department of Medical Laboratory Science, University of Benin Teaching Hospital, Benin, Nigeria
2 Benin City, Edo State, PCR Laboratory, University of Medical Sciences Teaching Hospital, Akure, Ondo, Nigeria
3 Department of Medical Microbiology, University of Benin Teaching Hospital, Benin, Nigeria
4 Department of Animal and Environmental Biology, University of Benin Teaching Hospital, Benin, Nigeria
5 Department of Anatomy, University of Benin, University of Benin Teaching Hospital, Benin, Nigeria

Date of Submission21-Feb-2020
Date of Decision21-Sep-2020
Date of Acceptance13-Jan-2021
Date of Web Publication26-Mar-2021

Correspondence Address:
Frederick Olusegun Akinbo
Department of Medical Laboratory Sciences, University of Benin, Benin
Nigeria
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/sjhs.sjhs_79_20

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  Abstract 


Background: West Africa includes the most endemic areas in the world with Nigeria being one of the largest countries of West Africa that has been reported to have a high incidence of onchocerciasis. Aim: The aim of this study was to determine Onchocerca volvulus infection among ivermectin-treated population in Ekpan community, Edo State, Nigeria. Setting and Design: A total of 105 participants including 60 males and 45 females with an age range of 15–81 years were recruited in the study. Random sampling technique was employed in the recruitment of participants. Materials and Methods: Two skin snip specimens were taken from the left and right iliac crests of each participant into a microtube containing physiological saline. The skin snips were processed using standard technique and examined microscopically for microfilariae of O. volvulus. Statistical Analysis: The data collected were analyzed using the Chi-square (X2) test and odd ratio. The statistical package used was GraphPad INSTAT. Results: An overall prevalence of 74.3% of O. volvulus infection was observed among ivermectin-treated subjects in Ekpan. Age, occupation, noncompliance of ivermectin treatment, and source of water significantly affected the prevalence of O. volvulus infection among ivermectin-treated population in Ekpan (P < 0.05). Conclusion: Effective distribution of ivermectin and strict compliance of ivermectin treatment are advocated as these efforts will go a long way at controlling as well as reducing the effects of onchocerciasis in this community.

Keywords: Edo state, ivermectin treatment, onchocerciasis


How to cite this article:
Akinbo FO, Olawale JO, Omoregie R, Okaka CE, Emokpae MA, Eze GI. Onchocerca volvulus infection among ivermectin-treated population in a rural setting in Edo State, Nigeria. Saudi J Health Sci 2021;10:65-9

How to cite this URL:
Akinbo FO, Olawale JO, Omoregie R, Okaka CE, Emokpae MA, Eze GI. Onchocerca volvulus infection among ivermectin-treated population in a rural setting in Edo State, Nigeria. Saudi J Health Sci [serial online] 2021 [cited 2021 Apr 14];10:65-9. Available from: https://www.saudijhealthsci.org/text.asp?2021/10/1/65/311960




  Introduction Top


Onchocerca volvulus infection is an insidious nonfatal filarial disease that has resulted in blindness, lifelong human suffering, and grave socioeconomic problems.[1] Onchocerciasis is a disease of the warm tropical environment where the black flies that vector the microfilariae (mf) live under conditions that are favorable for their development throughout the year.[2] The disease is described as a disease of the future because as the development of hinterlands proceed, especially as dams and water projects increase, it will cease to be a disease affecting only small, isolated, poverty stricken and primitive communities in the bush and will become more and more a threat to sophisticated development personnel and other such workers in Africa.[3]

West Africa includes the most endemic areas in the world with Nigeria being one of the largest countries of West Africa that has been reported to have a high incidence of onchocerciasis infection.[4] An estimated prevalence of 27% of nearly 200 million people are at risk globally and Nigeria has been reported as the most endemic country in the world for onchocerciasis.[5] Edo State has been observed to be endemic for onchocerciasis when compared with other parts of Nigeria probably due to poor mass drug administration coverage.[6],[7],[8] The main goal of African Program for Onchocerciasis Control (APOC) is to reduce the public health and socioeconomic problems of onchocerciasis with a period of 12–15 years using the strategy of yearly community-directed treatment with ivermectin (CDTI) in endemic areas. The use of ivermectin is highly effective, feasible, and offers a different approach to the control of onchocerciasis.[9] Community is the heart of the APOC strategy for controlling onchocerciasis. Community ownership of the distribution program is thought to be a major innovation for mass treatment and has been reported to be a cornerstone to the success of CDTI.[10] Ekpan is one of the communities in Uhunmwode Local Government Area, Edo State, where onchocerciasis has been reported over the years. Wagbatsoma and Aisien[11] evaluated the knowledge, attitude, and perception of onchocerciasis after 3 years of ivermectin distribution in Ekpan community. Similarly, Aisien et al.[12] investigated the prevalence of onchocerciasis among children aged 0–15 years in Ekpan using nodular index. Ivermectin is known to be the only available drug for mass treatment of onchocerciasis, which has been used for nearly 2 decades in Ekpan community to reduce the transmission of the disease. Persistent clinical manifestations have been reported after years of ivermectin treatment in this community. Information on the detection of O. volvulus infection among ivermectin-treated population in Ekpan community is lacking. Against this background, this study was conducted to determine O. volvulus infection among ivermectin-treated population in Ekpan community, Edo State, Nigeria.


  Materials and Methods Top


Study area

The study was conducted at Ekpan in Uhunmwode Local Government Area, Edo State, Nigeria. Ekpan is situated between longitudes 5° 56. 660'E and latitude 6° 43.210'N. The occupation of the inhabitants of this community is farming and the only source of water supply is the Ekpan River which provides the ideal breeding site for Simulium flies because of its fast flowing nature. The estimated population of Ekpan-Irhue is 1311.[13] Advocacy visits were paid to the head of the community in company of some staff of the Edo State Ministry of Health, Benin City, and dates were agreed upon for the commencement of specimen collection. The Ethics and Research Committee of the Ministry of Health, Benin City, Edo State, approved the protocol of the study.

Study population

One hundred and five subjects including 60 males and 45 females were recruited in the study. The age of the subjects ranged from 15 to 81 years. Participants who consented to be recruited were included, whereas those who refused consent were excluded from the study. Informed consent was obtained from each participant before specimen collection. A well-structured questionnaire was administered to each participant to collect biodata, sociodemographic characteristics, and ivermectin treatment before specimen collection. Random sampling technique was utilized in the study. A well-structured questionnaire was administered to each participant before specimen collection.

Physical examination

Physical examination was conducted by a physician on participants who consented to participate in the study behind translucent shield. Participants were examined for the presence of the characteristic subcutaneous onchocercal nodules by partially disrobing and palpated around the lower ribs and back, waist, iliac crest, sacrum, hips, and legs by a medical doctor. The visual acuity at far and near distance was examined and ability to count figures at distance of 6 m was tested by an optometrist. The eye was examined further with an ophthalmoscope. The skin was examined for papular rashes and depigmentation (leopard skin). The papular rashes and leopard skin were reported as present or absent on examination of the limbs. Pruritus was confirmed based on the responses from subjects and reported as present or absent.

Specimen collection

Skin snip specimens were collected from each participant. Two skin snip specimens were taken from the left and right iliac crests of each participant into a microtube containing physiological saline. Briefly, the skin over the left and right iliac crests was disinfected and blood-free skin snip was taken using a sterile needle and surgical blade[14] and transferred to a microtube containing fresh physiological saline. This preparation was allowed to incubate for 4 h at room temperature and centrifuged at 1000 rcf for 5 min. The deposit and the skin snips were examined microscopically for mf of O. volvulus.

Data analysis

The data collected were analyzed using the Chi-square (X2) test, odds ratio, and standard deviation. The statistical package used was GraphPad INSTAT.


  Results Top


Out of the 105 subjects examined, 78 (74.3%) had O. volvulus mf. The prevalence of mf observed in the skin was similar in both sexes (male = 76.67%; female = 71.11%). In addition, gender did not affect the prevalence of O. volvulus infection (OR = 1.335, 95% CI = 0.5538–3. 217; P = 0.6752). Age significantly affected the prevalence of O. volvulus infection (P = 0.0003) with participants who are 46–61 years being the most infected (93.54%), followed by 31–45 years (81.48%) and 62 years and above (68.96%), and the least infection was observed among the 15–30 years. Participants who are married had the highest prevalence (76.47%); however, being married did not strongly affect the prevalence of O. volvulus infection in our study area (P = 0.5602). Subjects with primary education were observed to have the highest infection rate (80%), but having a primary education did not affect significantly the prevalence of O. volvulus infection in Ekpan (P = 0.4652). Furthermore, family size did not strongly impact on O. volvulus infection among ivermectin-treated population in Ekpan (P = 0.1170). Participants who are farmers were the most infected by O. volvulus (83.33%). In addition, occupational status significantly affected the prevalence of O. volvulus infection in Ekpan community. Noncompliance of ivermectin treatment strongly associated with the prevalence of onchocerciasis among residents of Ekpan community (odds ratio [OR] = 0.4361; 95% confidence interval [CI] = 0.2455–0.7747; P = 0.0065). Source of water strongly associated with O. volvulus infection among the subjects in Ekpan with those that use the Ekpan River as their source of water having the highest infection (87.50%) (OR = 14.875; 95% CI = 5.100–43.383; P < 0.0001) [Table 1].
Table 1: Risk factors affecting the prevalence of onchocerciasis among ivermectin-treated population in Ekpan community

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  Discussion Top


O. volvulus infection is a serious health and socioeconomic problem.[15] The disease is a major problem among rural communities living in proximity to rivers in Sub-Saharan African Countries.[16] Ivermectin is the drug of choice for treatment and has been in Ekpan community for almost 2 decades. There has been no study to determine the detection of O. volvulus after several rounds of ivermectin treatment in Ekpan; hence, this study was conducted.

A prevalence of 74.3% of O. volvulus infection was observed among participants in this study. The prevalence observed (74.3%) in this study is higher than the 13.50% reported by Manyi et al.[17] in Mkar-Gboko, Benue State, 32.8% observed in Ebonyi State by Nworie et al.,[18] and 54.2% in Ibarapa Local Government Area, Oyo State.[19] Based on the classification of onchocerciasis outbreaks[7], the prevalence of O. volvulus infection (74.3%) in Ekpan village may be classified as hyperendemic. As a result of ivermectin microfilaricidal effect, a single dose of 150 μg/kg brings about a rapid decrease in the density of the skin microfilaria in O. volvulus infection. The mf are reduced on average by 98% after 2 weeks and by 99% after 2 months.[20] Since ivermectin is known to have little macrofilaricidal effect and no effect on the embryogenesis, adult female worms continue to produce new mf following treatment with ivermectin. However, due to the embryostatic effect of ivermectin, those newly produced mf are not released and as such degenerate in the uteri of the female worms. Following several months, the embryostatic effect get waned and the mf can again be released and, thus, reinvade progressively the skin.[20] It is expected that repeated yearly ivermectin treatment should significantly reduce the number of mf when compared with what was observed after the first dose.[21] It was observed in our study that some participants avoided their yearly ivermectin treatment, which may be the reason for reinvasion of mf produced in the uteri of the female worms to the skin. This may partly be responsible for the prevalence observed in our study. Other reasons for the hyperendemicity observed in our study area may have been continuously bitten by Simulium damnosum on the farms, frequent visit to the river which is the only source of water in the village, and perhaps, the noncompliance of ivermectin treatment by the subjects.

In rural settings, males are usually thought to be more involved in farming and hunting as they play a major role of providing for their family and as such exposes them more to the bite of S. damnosum than their female counterparts who may be confined to domestic chores in the house.[17] Furthermore, males are more likely to work on the farm with their body exposed to the bite of S. damnosum.[18] Surprisingly, gender did not significantly affect the prevalence of onchocerciasis among the subjects examined in Ekpan (P = 0.6752) as both sexes presented with similar prevalence (male = 76.67%; female = 71.11%). This observation is in tandem with the finding of Manyi et al.[17] in Mkar-Gboko, Benue State. This finding may mean that both sexes are exposed almost equally to the vector of this parasite.

The 46–61 years' age group had the highest prevalence (93.54%) of onchocerciasis followed by 31–45 years (81.48%). In addition, age significantly affected the prevalence of O. volvulus infection among participants in Ekpan (P = 0.0003). This finding is in agreement with the report of Nworie et al.[18] who observed a higher rate of onchocerciasis in the 40–49 years' age group. The reason for our finding may be due to the fact that the major occupation of the residents of Ekpan is farming, and therefore, the age groups (31–45 and 46–61 years) where we observed a higher rate of infection represent the active age groups of individuals who have been involved in farming for some time and as such had continuously been bitten by the vector flies.

Participants that are married presented with the highest prevalence of O. volvulus infection (76.47%) when compared with single (66.67%) and widowed (62.50%) individuals. In addition, marital status did not significantly affect the prevalence of O. volvulus infection among ivermectin-treated population in Ekpan (P = 0.5602). Subjects with primary education had the most remarkable infection of O. volvulus among ivermectin-treated population in Ekpan. Furthermore, educational status did not strongly affect the prevalence of O. volvulus infection in our study (P = 0.4652). Family size did not also strongly affect significantly the prevalence of O. volvulus in Ekpan (P > 0.05).

In our study, occupation significantly affected the prevalence of onchocerciasis (P = 0.0129) with participants who are farmers having the highest prevalence (83.33%). This observation is consistent with the report Manyi et al.[17] who observed a higher prevalence of onchocerciasis among farmers. Farming exposes people to continuous risk of S. damnosum bites and subsequently O. volvulus transmission throughout their lives.[18] This may be the reason for our finding.

In rural settings, where health systems are weak and underresourced, the community-directed treatment strategy is proving to be one of the Africa's most successful ways in reducing disease at low cost.[22] Ivermectin treatment coverage was high in our study area; however, compliance to treatment was very low. In this study, noncompliance to ivermectin treatment strongly associated with the prevalence of onchocerciasis (OR = 0.4361; 95% CI = 0.2455–0.7747; P = 0.0065) with those who did not comply with ivermectin treatment regimen having the highest prevalence of onchocerciasis (46.66%) when compared with ivermectin treatment compliant subjects (27.62%). Our finding suggests that the drug is distributed to individuals but majority missed the treatment rounds for various reasons. The need to emphasize strict compliance to ivermectin treatment regimen annually to effectively reduce the mf load for transmission and its associated sequelae is advocated.

The breeding of S. damnosum is known to require fast running water body. The Ekpan River which is the major source of water in this community is situated close to the residential settlement in the village and allows the breeding of the vector as a result of which residents of the community are bitten freely by the vector fly. Participants who use the river as the source of water were more infected (87.50%) than those that use rain/well water (32%). Furthermore, source of water strongly associated with the prevalence of O. volvulus infection among ivermectin treated subjects in Ekpan (OR = 14.875; 95% CI = 5.100–43.383; P < 0.0001). In this study, participants who use river water as a source of water have a 5–43-fold increased risk of acquiring O. volvulus infection.


  Conclusion Top


An overall prevalence of 74.3% of O. volvulus infection was observed among ivermectin-treated subjects in Ekpan. Age, occupation, noncompliance of ivermectin treatment, and source of water significantly affected the prevalence of O. volvulus infection among ivermectin-treated population in Ekpan (P < 0.05). As a result of increasing prevalence of O. volvulus infection in Ekpan following several rounds of ivermectin treatment, there is a need to determine if the parasite is developing resistance to ivermectin or there is a genetic diversity of the species of O. volvulus in this community.

Acknowledgments

The authors would like to appreciate the staff of the Edo State Ministry of Health, Epidemiological Unit, Benin City, for their cooperation and assistance in getting the Community Head to support our study. We also acknowledge all the participants who consented to participate in the study. Drs. E. Imafidon and A. Onuyor are also appreciated for their involvement in screening the participants.

Financial support and sponsorship

We received financial support from the Tertiary Education Trust Funds (TETfunds), in connection with this research. The TETFund is a National Research Grant in Nigeria to tertiary schools.

Conflicts of interest

There are no conflicts of interest.



 
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