Journal of Parasitology Research
Volume 2019 (2019), Article ID 7596069, 8 pages
https://doi.org/10.1155/2019/7596069

Research Article

Transmission Dynamics of Urogenital Schistosomiasis in the Rural Community of Ebonyi State, South Eastern Nigeria

F. N. Afiukwa,¹ D. E. Nwele,² O. E. Uguru,³ G. A. Ibiam,⁴ C. S. Onwe,² A. U. Ikpo,⁵ N. B. Agumah,¹ and O. F. Odoemena⁶

¹Department of Applied Microbiology, Faculty of Science, Ebonyi State University Abakaliki, Nigeria
²Department of Applied Biology, Faculty of Science, Ebonyi State University Abakaliki, Nigeria
³Department of Medical Microbiology, Faculty of Basic Medicine, Ebonyi State University Abakaliki, Nigeria
⁴Department of Medical Laboratory Sciences, Faculty of Health Sciences Ebonyi State University Abakaliki, Nigeria
⁵Department of Parasitology and Entomology, Nnamdi Azikiwe University Awka, Nigeria
⁶Department of Human Anatomy, Faculty of Basic Medicine, Ebonyi State University Abakaliki, Nigeria

Correspondence should be addressed to D. E. Nwele; davideolink@gmail.com

Received 2 July 2018; Revised 28 September 2018; Accepted 18 October 2018; Published 1 January 2019

Academic Editor: Bernard Marchand

Copyright © 2019 F. N. Afiukwa 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.

Abstract.

This study accessed the dynamics of urogenital schistosomiasis transmission in Nkalagu Community. A total of 500 mid-day urine samples were collected and transported to Microbiology Laboratory, Ebonyi State University, for analysis. 10ml each of the urine samples was centrifuged at 2500 rpm for 5 minutes. Transmission potential of snail intermediate host of Schistosomes collected from different sampling station at the transmission sites within the study community was equally accessed. The snail species collected were placed individually into a clean beaker with little quantity of water and then subjected to shedding light for 2 hours. Data obtained were entered in excel spread sheet and analyzed using chi square test. The result obtained shows that 205 (41%) out of 500 individuals examined were excreting S. haematobium ova in their urine. The highest prevalence of infection (23%) was found among 11-20-year age groups. Males were more infected (25.4%) than their female counterparts (15.6%), although this was not statistically significant (p > 0.05). A total of 283 snails belonging to two Bulinus species (B. globosus and B. truncatus) were collected from the four sites sampled. Bulinus globosus recorded the highest species abundance (177) with the highest occurrence in site A. 52 (18.4%) out of 283 snails collected were infected with cercariae, and the highest cercariae infection (12.0%) was recorded among B. globosus. With prevalence of 41% among the human population and the prevalence of 18.4% patent infection among the snail intermediate hosts, urogenital schistosomiasis is still a public health problem in the study area and falls within the WHO classification of endemic area. Public health campaign is recommended in order to educate the people on the mode of transmission and control of the disease.

1. Introduction

Urinary schistosomiasis is a parasitic disease caused by the blood fluke of the genus Schistosoma. The disease is endemic in 76 countries in the Middle East and most of the African countries [1]. It is one of the major public health problems facing humanity, with severe and economic consequences [2]. It is the most prevalent of waterborne diseases [3]. Human waste in water containing intermediate hosts is the single most important epidemiological factor in schistosomiasis transmission as well as the availability of suitable snail host [4]. The transmission of schistosomiasis is associated with water development projects such as dams for irrigation systems and fish-farming, as the snail intermediate hosts of the parasites breed in them and human water contact also takes place in such water body [5]. Urinary schistosomiasis being a water-based disease is spread through contact with water in which snail habouring and shedding the infective stage (cercariae) of the parasite (schistosome) are present [6, 7]. As with other zoonotic infections, urinary schistosomiasis has a natural habitat in a well-defined ecosystem. The parasite, intermediate hosts, and the human host form an association within which the parasite reproduces and is disseminated [8].

Nigeria is one of the countries known to be highly endemic for urinary schistosomiasis with more than 100 million people at risk and about 25 million already infected [1, 9]. School aged children are at high risk of infection and prevalence usually peaks between the ages of 8 and 15 years [10–12]. As a result of low level of resistance and intensive water contact when playing and swimming, children aged between 10 and 15 years are the most heavily infected [7, 13]. Increased population movements help to spread the disease, and Schistosomiasis is now occurring increasingly in peri-urban areas in endemic countries [14].

Typical signs of urinary schistosomiasis are macro- and microhaematuria, proteinuria and leukocyturia [11, 15] and the risk of haematuria, dysuria, nutritional deficiencies, lesion of the bladder, kidney failure, and child growth retardation are well established [16].

Human infection by Schistosomes frequently occur in stable foci and is dependent on snail infection and contact patterns of humans with water infested with cercariae [17]. The risk of infection in these transmission sites may be routinely estimated by detecting infected snails capable of shedding cercariae. However, since seasonal fluctuations exist in snail population densities, infection rates, and cercarial output, information on both snail infection and presence and distribution of cercariae is required for evaluating the risk of infection. Information on presence of cercariae in water is particularly important when only one of many snails is infected yet capable of shedding enough cercariae to maintain high endemicity [18].

2. Study Area and Population

The study was carried out for a period of 12 months in Nkalagu Community, a Schistosomiasis endemic area in Ebonyi State. Nkalagu Community is made up of five (5) villages: Ishiagu, Amanvu, Uwule, Imoha, and Akiyi. The geographical coordinate of the study area lies between longitude 54°E and latitude 60°N. The climate of the study area is tropical with mean daily temperature of 30 ± 5°C for the most of the year. The annual rainfall is between 1900 and 2200mm, with wet and dry seasons. The vegetation is typically rainforest. Several freshwater habitats intersect the study area, some of which include ponds, streams, dams, and rivers. These water bodies form the major source of water supply to the residents of the study area. During both wet and dry seasons, activities increase around these water bodies as people converge to use them for domestic, agricultural and recreational activities all of which could predispose them to urinary schistosomiasis. The study area was selected based on previous report on schistosomiasis prevalence as well as laboratory/confirmatory evidence of the disease in the area during preliminary survey. All individuals resident in the study area for the past one year before the study were included for participation.

3. Ethical Consideration and Consent

Ethical clearance was obtained from Ebonyi State Ministry of Health who issued a letter permitting the study to the community leaders. The study participants were informed about the purpose, procedures, and potential risk and benefits of the study and were invited to approve their participation in the study. A written informed consent was signed by each study participant at the beginning of the study.

4. Study Population and Design

This present study includes 500 individuals of different age groups and sex who consented to participate in the study. The participants were selected using random sampling technique on a house to house basis as described by Nwosu et al. [19].

A 20ml of clean catch, midstream urine samples was collected in autoclaved wide mouthed, leak proof universal containers by the study participants themselves as described by WHO [20] and Uneke et al. [9]. Samples were collected between 10.00 am and 14.00 hours, labeled with unique identifiers and transferred to the laboratory in a cold box with ice packs. The urine samples were processed 1-2 hours after collection.

5. Laboratory Analysis of Sample

In the laboratory, 10ml terminal urine was centrifuged at 2,500 revolution per minute (rpm) for 5 minutes in order to concentrate eggs of schistosome as described by Cheesbrough [21]. The urine sedimentation technique described was used to detect the presence of S. haematobium ova in the urine samples mounted under microscope. Intensity of the infection in each case was reported as the number of ova/10ml of urine and was categorized as light infection (<50 ova/10ml of urine) or heavy infection (>50 ova/10ml of urine) [21].

6. Snail Sampling Technique/Procedure

The sampled rivers (Abashi and Edenvu) for this study were divided into different sampling stations (A, B, C, and D) on the basis of accessibility and variations in site ecology. Each of the sampling stations was sampled on monthly basis for two seasons (wet and dry seasons).

Two major techniques were adopted for the snail sampling; the scooping technique and the manual hand picking technique. Scooping net technique involves the use of scooping net in collecting the snails. The scoop net was lowered under the vegetation at the bank of the river and scooped in order to catch the snails attached to the shrubs as described by Oguoma et al. [22] and Ivoke et al. [8]. This was repeated severally at random in different locations on each day of sampling. In manual hand picking, long forceps were used to pick snails resting on vegetation and under the stream. Snails were also picked with hands covered with gloves to avoid direct contact with infested water and snails as described by Oguoma et al. [22]. All snails collected each day of sampling at each station were kept in a prelabeled transparent bucket containing water from the site. The sample was transported to the laboratory for identification and examination using key provided by Brown, [23] and Okafor and Obiezue, [24]. The identified snail species was later confirmed by Senior Parasitologist in the Department of Applied Biology of the Ebonyi State University.

7. Laboratory Examination of Snail for Cercariae Shedding

In the laboratory, the collected snails were placed individually into a clean 100ml beaker with little quantity of clean water. Each beaker was then placed under a 100 watt bulb (shedding light), as described by Okafor [25] and Ivoke et al. [8] to stimulate the emergence of the cercaria if present in the snail. The beaker was allowed to stay under the shedding light for about 2hrs after which the snail was transferred to another beaker and the sheded cercaria counted. The process was repeated until no cercaria was coming out of the snail again. Adequate care was taken during this process not to overheat and kill the snails. In the absence of shedding light, direct sunlight was used to achieve the same purpose. Beakers containing snail and water were placed directly under the sun and monitored for the emergence of cercaria as described by Okoli and Iwuala [26]. All cercaria encountered during the process was counted and recorded.

8. Data Analysis

Data collected was double entered in Microsoft excel and checked for consistency and analyzed using SPSS version 20.0. The S. haematobium infection prevalence, defined as the percentage of individual with S. haematobium eggs in urine, was calculated. Chi square test was used to determine statistical difference between two variables.

9. Results

A total of 500 participants, comprising both males and females, were included in this study. The overall infection prevalence was 41% with the highest infection prevalence (23%) occurring among age group 11-20 years and was closely followed by ≤10 years age group (12.6%). The least infection prevalence (1.8%) was recorded among 31-40 years age groups. Statistically there was no significance difference in the prevalence of infection among the age groups (X²= 1.02; df = 5, P> 0.05) (Figure 1). See Figure 3 for the image of the S. haematobium ova recovered from the urine sample.

Figure 1: Prevalence of urogenital schistosomiasis by age.

The result obtained on the distribution of the infection by sex showed that the overall prevalence of infection was highest among males (25.4%) than their female counterparts (15.6%). However, there was no significant difference in the prevalence in both sexes (P> 0.05) (Figure 2).

Figure 2: Prevalence of infection by sex.

Figure 3: Ova of S. haematobium recovered from urine sample.

A survey of the abundance and species distribution of the snail intermediate host of urogenital Schistosomiasis around the fresh water bodies in the study community showed a total snail population of 283 snails belonging to two species (Bulinus globosus and Bulinus truncatus). The highest snail population was recorded among B. globosus (Figure 4).

Figure 4: Distribution of different snail species in different sites sampled.

The distribution of snail species in the different stations sampled varied considerably with the site and months of the survey. The highest number of snail species was encountered in site A (134), while site D recorded the least number of snail (36). Monthly abundance also shows that more snails were collected in the months of June, August, and October when water current capable of dislodging snails was reduced while least snail number (6, 10 and 18) was found between February, March, and April, respectively, due to a decrease in the volume of the river. No snail was collected in the month of January (Table 1).

Table 1: Monthly abundance of Bulinus species in various sites sampled.

Sampling months
No. of snail species
No. per sampling sites

A
B
C
D
Total

Jan.
0
0
0
0
0
0

Feb.
6
6
0
0
0
6

Mar.
10
5
1
3
1
10

Apr.
18
7
5
4
2
18

May
40
17
8
10
5
40

Jun.
54
21
9
19
5
54

Jul.
28
16
2
7
3
28

Aug.
51
28
6
17
0
51

Sept.
25
16
0
9
0
16

Oct.
50
18
11
1
20
50

Total
283
134
42
71
36
283

Figure 5 shows the percentage output of cercariae shedding by different snail species when subjected to shedding light. Out of the 283 snails collected and subjected to shedding light, only 52, (18.4%) were shedding cercariae with the highest number of snails shedding cercariae, recorded among Bulinus globosus, 34(12.0%) while the least number of snail shedding cercariae was found among B. truncatus, 18(6.4%). The image of the cercariae captured from the microscope is show in Figure 6.

Figure 5: Percentage output of cercariae shedding by different snail species.

Figure 6: Image of cercariae taken from the microscope.

10. Discussion

Studies have shown that urinary Schistosomiasis is a major health problem in the rural areas of the Middle East and most African countries [20]. It remains one of the major health problems facing developing countries. The endemicity of the disease in many rural areas was attributed to poor living conditions, ignorance, inadequate sanitation, inadequate water supply, personal and environmental hygiene, and water contact activity with snail infected river, streams, and ponds [20].

This study recorded Schistosoma haematobium prevalence of 41% in the community studied. The result suggests that the study area falls within the WHO classification as endemic area [2]. The result is consistent with many other studies in Ebonyi State which shows that the disease is endemic in many rural communities of the state [9, 19, 27, 28]. However, the prevalence recorded in this present study is higher than the 22.1% reported by Anosike et al. [28] in the rural communities of Ebonyi State. It was equally higher than the 17.5% reported by Nwosu et al. [29] in Ezza North Local Government Area of Ebonyi State and was slightly lower than the 47.9% reported in Ohaukwu Local Government Area by Uneke et al. [9] in 2006. The major factors that contribute to high prevalence of urogenital schistosomiasis in any rural community are poor environmental sanitation, inadequate and indiscriminate disposal of human excreta (especially around freshwater bodies), and behavioural activities that brings people in contact with infested water bodies where transmission occurs. Uneke et al. [9] reported that low literacy, lack of basic amenities, inadequate and indiscriminate disposal of human sewage, and high water contact activity with snail infested pond, river, and stream may have been responsible for high endemicity of urinary schistosomiasis particularly in Ohaukwu.

The age prevalence of urogenital schistosomiasis as recorded in this study showed variation among different age groups studied with age group 11-20 years, recording the highest infection prevalence of 23%, and was followed by ≤10 years age groups with the prevalence of 12.6%. The high prevalence among 11-20 age groups indicates that they are the most active age group frequently engaging in activities that brings them in contact with infested water bodies which are possible transmission sites. This finding agrees with the earlier works of Okpala et al. [13] who equally reported highest prevalence among 11-15 age groups. Similarly, Okoli and Odaibo [30] reported school aged children especially those within the age group 11-15 as having the highest prevalence of S. haematobium infection. Nwosu et al. [19] equally reported highest prevalence among age group 11-20 years. The result of this study and other reports therefore indicate that transmission is usually high among children which are mainly due to their role in contamination of aquatic environment. According to Anosike et al. [31], children are the most infected group of people in endemic areas, thus contributing significantly to the potential contamination of the aquatic environment. The first two decades of life have been identified as the age of active life; hence increased human activity increases predisposition of people in this age group to infection especially through increased water contact activities [19]. The prevalence of infection recorded among ≤10 years age group could be due to early exposure to contaminated water as earlier reported by Nwosu et al. [19],

Regarding the prevalence of infection in relation to sex, this study showed that males were more infected with 25.4% prevalence than their female counterparts (15.6%). The high prevalence among males may be attributed to their behavioural practices which bring them in contact with the infested water than their female counterparts who usually engage more in domestic activities. Similar observations have been reported by Uneke et al. [9], Nwosu et al. [19], and Nwele et al. [7] in their separate studies. However, other studies reported that sex related prevalence is significant but could differ due to some variations in behavioural practices regarding water contact [32].

Survey of freshwater snail intermediate hosts around the river where transmissions takes place identified two snail species of Bulinus (B. globosus and B. truncatus). All snails recorded in this study have been previously reported in other parts of Nigeria [33].

There was considerable variation in the abundance of the snail species within the months of study. The highest number of snails was collected in the months of June, August, October, and May while the least number was seen in the month of February. The relative abundance of snails from May to October could be attributed to the availability of food which increases the growth of aquatic plants as well as the stability in water velocity. A drop in the snail population in the months of July and September indicates an increase in amount of rainfall with consequent increase in water current which is capable of sweeping snail population. Ndifon et al. [34], in his study, identified rainfall as the major factor influencing the availability of aquatic snails.

The snail population recorded in this study varied greatly with the different sites sampled with site A recording the highest snail abundance. The low number of snail recorded in sites B and D may have been occasioned by rainfall through flooding and subsequent flush out of snails from their habitats or by the rapid elevation of water levels resulting in the snails remaining submerged in the rivers. Several researchers in different part of the world have been able to demonstrate the usefulness of rainfall in increase or decrease of snail populations [33, 35–37].

The overall percentage of snail species shedding cercariae stood at 18.4% and this was lower than that reported by Ayanda [38], who recorded overall cercariae prevalence of 35.7%. The cercarial shedding was highest among B. globosum with prevalence of 12.0% while B. truncatus recorded the least prevalence of 6.4%. This, however, did not agree with the earlier report of Ayanda [38], who recovered 35.7% cercaria all from B. globosus from the stream of samara, in Zaria. The recovering of cercariae from the snail species collected is an indication that transmission is taking place in the study area and many individuals in these communities are not aware of the dangers associated with contact to these water bodies and therefore could be at greatest risk of infection. Though there was no particular trend in the variation of prevalence, it could be said from the result that increase in infected snail populations may result in an increase in the infection of human host by Schistosome cercariae resulting from their behavioural practices capable of bringing them in contact with the infested water. Although mortality due to schistosomiasis may be low, the disease imposes a heavy burden upon the health and wellbeing of individuals [39, 40].

11. Conclusion

The occurrence of cercaria in the collected snails indicates the presence of urinary schistosomiasis in the study area and this equally indicates that people making contact with the water where these snails were collected could be at risk of infection. Efforts should be geared towards educating the people of this community on the possible health risk involved when exposing their body to the river, as well as controlling the snail intermediate host.

Data Availability

No data were used to support this study.

Conflicts of Interest

We hereby declare that no conflicts of interest exist among us.

Authors’ Contributions

We declare that this work was done by the authors named in this article and all liabilities pertaining to claims relating to the contents of this article will be borne by the authors. F. N. Afiukwa and D. E. Nwele conceived and designed the experiment. D. E. Nwele, A. U. Ikpo, and O. E. Uguru carried out the field collection of sample. D. E. Nwele, G. A. Ibiam, F. N. Afiukwa, and N. B. Agumah performed the laboratory analysis of sample. D. E. Nwele, C. S. Onwe and A. U. Ikpo identified the snail species. F. N. Afiukwa, D. E. Nwele, and O. F. Odoemena carried out quantitative analysis of data and result computation. F. N. Afiukwa and D. E. Nwele wrote the first draft of the manuscript while all authors read, corrected, and approved the final manuscript.

Acknowledgments

We thank Dr. C. A. Afiukwa for his useful contributions and also for taking time to edit our manuscript. We equally owe thanks to the community leaders for their unalloyed support and cooperation during the field sample collection.

References

L. Chitsulo, D. Engels, A. Montresor, and L. Savioli, “The global status of schistosomiasis and its control,” Acta Tropica, vol. 77, no. 1, pp. 41–51, 2000.

WHO, “Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO expert committee,” No. 912, WHO Technical Report Series, 2002.

World Health Organization, “Report of the WHO Informal Consultation on Schistosomiasis Control,” in WHO/CDS/CPC/SIP/992.2, World Health Organization, Geneva, 1998.

B. Robert, “Schistosomiasis,” in Tropical Disease Research Progress, pp. 29–36, 1993.

R. K. Klumpp and G. Webbe, “Focal, seasonal and behavioural patterns of infection and transmission of Schistosoma haematobium in a farming village at the Volta Lake, Ghana,” Journal of Tropical Medicine and Hygiene, vol. 90, no. 5, pp. 265–281, 1987.

M. F. F. Costa de Limae, R. S. Pocha, P. Fuhocoura, and N. Katz, “A 13-years follow-up of treatment and snail control in the endemic area for Schistosoma mansoni in Brazil, incidence and re-infection,” Bulletin of World Health Organization, vol. 7, no. 2, pp. 197–205, 1993.

D. Nwele, E. Afiukwa, C. Uhuo, G. Ibiam, and N. Agumah, “Human water contact activities and associated urogenital schistosomiasis in Nkalagu Community, Ebonyi State, Nigeria,” Nigerian Journal of Parasitology, vol. 38, no. 2, p. 153, 2017.

N. Ivoke, O. N. Ivoke, C. D. Nwani et al., “Prevalence and transmission dynamics of Schistosoma haematobium infection in a rural community of southwestern, Ebonyi State, Nigeria,” Tropical Biomedicine, vol. 31, no. 1, pp. 77–88, 2014.

C. J. Uneke, P. Oyibo, C. Ugwuoru, A. Nwanokwai, and R. Iloegbunam, “Urinary schistosomiasis among school age children in Ebonyi State, Nigeria,” The Internet Journal of Laboratory Medicine, vol. 2, no. 1, pp. 70–74, 2006.

I. A. Awogun, “A comparism of S. haematobium and S. mansoni among secondary school children in Ilorin, Kwara State,” Nigerian Journal of Parasitology, vol. 9, no. 11, pp. 51–54, 1990.

B. Gryseels, K. Polman, J. Clerinx, and L. Kestens, “Human schistosomiasis,” The Lancet, vol. 368, no. 9541, pp. 1106–1118, 2006.

M. E. J. Woolhouse, “Patterns in parasite epidemiology: The peak shift,” Parasitology Today, vol. 14, no. 10, pp. 428–434, 1998.

H. O. Okpala, E. Agwu, M. I. Agba, O. R. Chimezie, G. O. Nwobu, and A. A. Ohihoin, “A survey of the prevalence of Schistosomiasis among pupils in Apata and Laranto areas in Jos, Plateau State,” The Online Journal of Health and Allied Sciences, vol. 3, no. 1, pp. 1–4, 2004.

WHO, WHO Model Prescribing Information: Drugs Used in Parasitic Diseases, World Health Organization, Geneva, 1990.

D. J. Gray, A. G. Ross, Y.-S. Li, and D. P. McManus, “Diagnosis and management of schistosomiasis,” BMJ, vol. 342, no. 7807, Article ID d2651, 2011.

M. H. Mostafa, S. A. Sheweita, and P. J. O’Connor, “Relationship between Schistosomiasis and Bladder Cancer,” Clinical Microbiology Reviews, vol. 12, no. 1, pp. 97–111, 1999.

J. I. Alozie and J. Anosike, “Prevalence Of Urinary Schistosomiasis In Ozuitem, Bende Local Government Area Of Abia State, Nigeria,” Animal Research International, vol. 1, no. 2, pp. 77–80, 2004.

D. R. Yirenya-Tawiah, A. A. Rashid, G. Futagbi, I. Aboagye, and M. Dade, “Prevalence of snail vectors of schistosomiasis in the kpong head pond, Ghana,” West African Journal of Applied Ecology, vol. 18, pp. 40–45, 2011.

D. Nwosu, J. Anosike, B. Nwoke, and J. Uwaezouke, “Epidemiological assessment of vesical schistosomiasis in bende local government area of abia state, Nigeria,” Journal of Applied Sciences and Environmental Management, vol. 10, no. 2, pp. 55–60, 2006.

World Health Organization, Manual of Basic Techniques for a Health Laboratory, World Health Organization, Geneva, Switzerland, 2nd edition, 2003.

M. Cheesbrough, District Laboratory Practice in Tropical Countries, Cambridge University Press, Cambridge, UK, 2002.

V. M. Oguoma, N. D. Ugorji, K. V. Okolo, E. C. Mbanefo, and J. M. Umeh, “quatic snail species of two adjoining rivers in Owerri, Imo State, Southeastern Nigeria,” Animal Research International, vol. 7, no. 1, pp. 1125–1128, 2010.

D. S. Brown and T. K. Kristensen, A Field Guide to African Freshwater Snails I. West African species, Monograph of the Danish Bilharziasis Laboratory, Charlottenlund, 1993.

F. C. Okafor and N. R. Obiezue, “Freshwater snail host of trematode parasites in Nigeria,” Louis Chemz Printing Enterprise (Nig), p. 154, 2015.

F. C. Okafor, “Schistosoma haematobium cercariae transmission patterns in freshwater systems of Anambra State, Nigeria,” Angewandte Parasitologie, vol. 31, no. 3, pp. 159–166, 1990.

C. G. Okoli and M. O. E. Iwuala, “Studies on the prevalence of Schistosomahaematobium and the transmission potentials of the snail intermediate host Bulinus (physopsis) globosus in some riverine localities in Imo State,” in Proceedings of the International Journal of Environmental Health and Human Development, vol. 2, pp. 30–35, Nigeria, 2001.

J. C. Anosike, B. E. B. Nwoke, A. N. Okere, J. I. Alozie, U. O. Okoro, and D. C. Nwosu, “Endemicity of urinary schistosomiasis in the North Central Zone of Abia State,” International Journal of Environmental Health and human Development, vol. 2, no. 2, pp. 5–12, 2001.

J. C. Anosike, U. T. Oguwuike, B. E. B. Nwoke et al., “Studies on vesical schistosomiasis among rural Ezza farmers in the southwestern border of Ebonyi State, Nigeria,” Annals of Agricultural and Environmental Medicine, vol. 13, no. 1, pp. 13–19, 2006.

D. C. Nwosu, E. I. Obeagu, S. J. Ozims, M. C. Ezeama, and H. I. Uduji, “Prevalence of urinary schistosomiasis infection among primary school pupils,” International Journal of Current Microbiology and Applied Sciences, vol. 4, no. 5, pp. 1151–1157, 2015.

E. I. Okoli and A. B. Odaibo, “Urinary schistosomiasis among schoolchildren in Ibadan, an urban community in south-western Nigeria,” Tropical Medicine & International Health, vol. 4, no. 4, pp. 308–315, 1999.

J. C. Anosike, A. J. Njoku, B. E. B. Nwoke et al., “Epidemiology of urinary schistosomiasis in Ebonyi State Nigeria,” International Journal of Health and Human Development, vol. 3, p. 5962, 2002.

P. Verlé, F. Stelma, P. Desreumaux et al., “Preliminary study of urinary schistosomiasis in a village in the delta of the Senegal river basin, Senegal,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 88, no. 4, pp. 401–405, 1994.

R. F. Sturrock, O.-T. Diaw, I. Talla, M. Niang, J.-P. Piau, and A. Capron, “Seasonality in the transmission of schistosomiasis and in populations of its snail intermediate hosts in and around a sugar irrigation scheme at Richard Toll, Senegal,” Parasitology, vol. 123, pp. S77–S89, 2001.

G. T. Ndifon and F. M. A. Ukoli, “Ecology of freshwater snails in south-western Nigeria. I: Distribution and habitat preferences,” Hydrobiologia, vol. 171, no. 3, pp. 231–253, 1989.

D. Clercq, J. Vercruysse, M. Picquet et al., “The epidemiology of a recent focus of mixed Schistosoma haematobium and Schistosoma mansoni infections around the 'Lac de Guiers' in the Senegal River Basin, Senegal,” Tropical Medicine & International Health, vol. 4, no. 8, pp. 544–550, 1999.

S. O. Oladejo and I. E. Ofoezie, “Unabated schistosomiasis transmission in Erinle River Dam, Osun State, Nigeria: Evidence of neglect of environmental effects of development projects,” Tropical Medicine & International Health, vol. 11, no. 6, pp. 843–850, 2006.

J. Belot, S. Geerts, and M. Diouf, “Observations on the population dynamics of snail hosts for schistosomes in the delta of the Senegal river basin,” Journal of Molluscan Studies, vol. 59, no. 1, pp. 7–13, 1993.

O. Ayanda, “Prevalence of Snail Vectors of Schistosomiasis andtheir Infection Rates in two Localities within AhmaduBello University (A.B.U.) Campus, Zaria, Kaduna State, Nigeria,” Journal of Cell and Animal Biology, vol. 4, pp. 058–061, 2009.

World Health Organization (WHO), “The Control of Schistosomiasis,” Report of the WHO Expert Committee, Technical Report Series No 728, World Health Organization, Geneva, Switzerland, 1985.

A. Isabwe1, E. Ruberanziza, D. Mupfasoni, J. Ruxin, J. Clerinx, and P. T. White, “Potential for transmission of schistosomiasisin kayonza district,” Rwanda Medical Journal, vol. 69, no. 2, pp. 14–19, 2012.