Journal of Tropical Medicine

Journal of Tropical Medicine / 2020 / Article

Review Article | Open Access

Volume 2020 |Article ID 8850840 | https://doi.org/10.1155/2020/8850840

Tamirat Hailegebriel, Endalkachew Nibret, Abaineh Munshea, "Prevalence of Schistosoma mansoni and S. haematobium in Snail Intermediate Hosts in Africa: A Systematic Review and Meta-analysis", Journal of Tropical Medicine, vol. 2020, Article ID 8850840, 18 pages, 2020. https://doi.org/10.1155/2020/8850840

Prevalence of Schistosoma mansoni and S. haematobium in Snail Intermediate Hosts in Africa: A Systematic Review and Meta-analysis

Academic Editor: Pedro P. Chieffi
Received28 Jul 2020
Revised26 Aug 2020
Accepted28 Aug 2020
Published07 Sep 2020

Abstract

Background. Schistosomiasis is caused by Schistosoma mansoni and S. haematobium in Africa. These schistosome parasites use freshwater snail intermediate hosts to complete their lifecycle. Varied prevalence rates of these parasites in the snail intermediate hosts were reported from several African countries, but there were no summarized data for policymakers. Therefore, this study was aimed to systematically summarize the prevalence and geographical distribution of S. mansoni and S. haematobium among freshwater snails in Africa. Methods. Literature search was carried out from PubMed, Science Direct, and Scopus which reported the prevalence of S. mansoni and S. haematobium among freshwater snails in Africa. The pooled prevalence was determined using a random-effect model, while heterogeneities between studies were evaluated by I2 test. The meta-analyses were conducted using Stata software, metan command. Results. A total of 273,643 snails were examined for the presence of S. mansoni and S. haematobium cercaria in the eligible studies. The pooled prevalence of schistosome cercaria among freshwater snails was 5.5% (95% CI: 4.9–6.1%). The pooled prevalence of S. mansoni and S. haematobium cercaria was 5.6% (95% CI: 4.9–6.3%) and 5.2% (95% CI: 4.6–5.7%), respectively. The highest pooled prevalence was observed from Nigeria (19.0%; 95% CI: 12.7–25.3%), while the lowest prevalence was reported from Chad (0.05%; 95% CI: 0.03–0.13). Higher prevalence of schistosome cercaria was observed from Bulinus globosus (12.3%; 95% CI: 6.2–18.3%) followed by Biomphalaria sudanica (6.7%; 95% CI: 4.5–9.0%) and Biomphalaria pfeifferi (5.1%; 95% CI: 4.1–6.2%). The pooled prevalence of schistosome cercaria obtained using PCR was 26.7% in contrast to 4.5% obtained by shedding cercariae. Conclusion. This study revealed that nearly 6% of freshwater snails in Africa were infected by either S. haematobium or S. mansoni. The high prevalence of schistosomes among freshwater snails highlights the importance of appropriate snail control strategies in Africa.

1. Introduction

Schistosomiasis is one of the neglected tropical diseases (NTD) endemic in 78 countries and infects more than 229 million peoples in tropical and subtropical regions [1]. More than 90% of these cases are concentrated in Africa [2, 3]. The burden of the disease is even more severe in sub-Saharan Africa. Poor environmental sanitation and suitability of the climate conditions for snail intermediate host contribute to the high endemicity of the region. Schistosomiasis ranks second next to malaria from parasitic infection in terms of socioeconomic and health impact in tropics [4].

Human schistosomiasis is caused by Schistosoma mansoni, S. haematobium, S. japonicum, S. intercalatum, S. mekongi, S. malayensis, and S. guineensis [57]. Among these species, S. mansoni, S. haematobium, and S. japonicum are the major causes of human schistosomiasis globally [8]. Schistosoma mansoni and S. haematobium are widely distributed and the dominant cause of human schistosomiasis in Africa [5]. The endemicity of the disease in the region is linked with the availability of freshwater snail intermediate hosts.

About 350 species of freshwater snails are known to be medically or veterinary important [9]. Among these diverse snails, Biomphalaria, Bulinus, and Oncomelania snails [4] are the dominant snail genera that are involved in the transmission of human schistosomiasis. The Biomphalaria genus consists of B. pfeifferi, B. glabrata, B. sudanica, B. straminea, B. tenagophila, B. alexandarina, and B. choanomphala [10]. Biomphalaria snails serve as the intermediate host for S. mansoni, which is responsible for intestinal and hepatic schistosomiasis. Biomphalaria pfeifferi is the most common and widely distributed snail intermediate host for S. mansoni in Africa.

Bulinus consists of 37 recognized species, which is grouped mainly into four species groups, namely, Bulinus africanus, B. forskalii, B. truncates/tropicus, and B. reticulatus [10, 11]. Bulinus snails serve as intermediate hosts for S. haematobium, which is responsible for urinary schistosomiasis. Oncomelania snails consist of only a few species mainly reported from Asia. The most common snail intermediate host for S. japonicum is Oncomelania hupensis, which is found in China, the Philippines, Indonesia, and also Japan [12].

The prevalence of human schistosomiasis is varied greatly in African countries depending on the level of environmental sanitation and the suitability of the area for the snail intermediate hosts, as well as the type of snail in the area. Similarly, the prevalence of schistosomes cercaria in snail intermediate hosts is varied in different locations within the same country and also from country to country in Africa. Several epidemiological studies are available on the types and prevalence of human infecting schistosomes among snail intermediate hosts in Africa. However, up to this time, there has not been any single estimate of the prevalence of S. mansoni and S. haematobium in snail intermediate hosts in Africa that could be used by African policymakers and international organizations working on the prevention and control of schistosomiasis in the continent. Therefore, this study aimed to provide summarized data on the prevalence and geographical variations of S. mansoni and S. haematobium cercaria among freshwater snails in Africa.

2. Methods

2.1. Search Strategies

Relevant literature was systematically searched from online public databases (PubMed Central, Science Direct, and Scopus) using the following key-words: “Schistosomiasis” OR “S. mansoni” OR “S. haematobium” OR “parasitological study” OR “schistosome intermediate host” OR “freshwater snails” OR “malacological survey” OR “Biomphalaria snails” OR “Bulinus snails” AND “Africa”. The systematic review and selection of relevant literature were conducted according to PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analysis) guidelines [13] (Table S1).

2.2. Inclusion and Exclusion Criteria

Literature published in English language from 1979 to June 2020 were extracted from online public databases. Original articles reporting the prevalence of human schistosome cercariae in freshwater snails in African countries were included in the analysis. The eligibility for the inclusion of a study in our analysis had to fulfill the following criteria: (a) it was published in English, (b) the study was carried out in Africa, (c) the number of examined and infected snails with either S. mansoni or S. haematobium were clearly stated, and (d) snail species were identified at least to a genus level. Studies that reported nonhuman schistosome and other trematodes species were excluded from the analysis. Besides, review articles and meta-analysis were excluded from the analysis.

2.3. Data Extraction Protocol

The data extraction protocol was prepared and evaluated by all authors. From each published article, we extracted the following information: author information, year of publication, study country, snail species, number of snails (collected, examined and infected), the prevalence of snail infection, the type of schistosomes reported, and methods of schistosome’s detection.

2.4. Quality of Individual Study and Assessment of Bias

The quality of studies included in the meta-analysis was assessed by using the Newcastle–Ottawa quality assessment scale (NOS) proposed by Wells et al. [14] (Text S1). The quality assessment tool consists of three parts. First, the selection of study groups graded on a scale containing five stars; mainly deals with methodological qualities of individual study. Second, comparability of groups graded on a scale containing two stars; deals with comparability of studies based on design and analysis. Third, outcomes graded on a scale containing three stars, mainly focused on the assessment of the outcome and statistical analysis. Two authors (TH and EN) independently assessed the quality of individual study, and disagreement was solved by a discussion with the third author (AM). The overall quality of the individual study was categorized as high quality (≥8 stars), moderate quality (6-7 stars), and low quality (≤5 stars) by the total number stars obtained as described elsewhere [15].

2.5. Publication Bias across Studies

The risks of publication bias across studies were assessed using funnel plot symmetry qualitatively. Egger’s and Begg’s test were used to determine the presence of publication bias across studies quantitatively.

2.6. Data Analysis

We used a forest plot to estimate the overall pooled effect size with their 95% confidence interval (CI). The heterogeneity among studies used for this meta-analysis was evaluated using the I2 test [16]. An I2- value lower than 25%, between 25% and 50%, and above 50% was regarded as low, moderate, and high heterogeneity, respectively [17]. Because of the high heterogeneity observed among the studies included in the meta-analysis, we used a random-effect model at 95% CI. To sort out the cause of heterogeneity, we used a subgroup analysis, sensitivity test, and meta-regression analysis. The data analysis was conducted using Stata software (version 14, STATA Corp College Station, TX), “metan” command.

3. Results

3.1. Search Results and Eligible Studies

A total of 2,995 relevant studies were screened from online public databases. Out of these studies, 976 articles were removed due to duplications while 1884 articles were excluded based on title and abstract screening. The remaining 135 full-text articles were assessed for eligibility. Of these, a total of 84 articles were excluded from the analysis based on specific exclusion criteria, and the remaining 51 articles were selected for this meta-analysis (Figure 1).

3.2. Characteristics of Subjects in the Eligible Studies

The eligible articles were obtained from 17 African countries: Angola [18], Benin [19], Burkina Faso [20], Burundi [21], Chad [22], Côte d’Ivoire [23, 24], Egypt [2530], Ethiopia [3136], Kenya [3739], Mali [40, 41], Niger [42, 43], Nigeria [4454], Senegal [55, 56], Sudan [57], Tanzania [5863], Uganda [6467], and Zimbabwe [68]. Unfortunately, there were no studies from other African countries that fulfilled the inclusion criteria. Characteristics of the eligible article to this meta-analysis are presented in Table 1.


AuthorYearCountrySnail speciesSnails examined (n)Infected snailsTotalSchistosoma speciesQuality score
Cercaria shedding (n)Prevalence (%)Screened by PCRPositive (n)Prevalence (%)Infected snails (n)Prevalence (%)

Sturrock et al. [39]1979KenyaB. pfeifferi938656.93656.93S. mansoni7
King et al. [30]1982EgyptBullines spp.431290.2190.21S. haematobium8
Lwambo [60]1988TanzaniaB. nasutus176461560.881560.88S. haematobium9
Gryseels [21]1991BurundiB. pfeifferi291992490.852490.85S. mansoni9
Bado et al. [40]1997MaliB. truncatus266--266228.30228.3S. haematobium8
B. globosus9077.8077.80S. haematobium
Kariuki et al. [37]2004KenyaB. nasutus110001221.201221.20S. haematobium8
Kazibwe et al. [66]2006UgandaB. stanleyi217159494.409494.40S. mansoni9
B. sudanica84522963.502963.50S. mansoni
Hussien et al. [29]2007EgyptB. alexandrina2070100.48100.48S. mansoni8
Labbo et al. [43]2007NigerB. forskalii945050.0550.05S. haematobium8
B. truncatus271255091.905091.90S. haematobium
Hussien et al. [25]2008EgyptB. truncatus837141.67141.67S. haematobium7
Odongo-Aginya et al. [64]2008UgandaB. choanomphala91941641.781641.78S. mansoni9
B. pfeifferi4173751.79751.79S. mansoni
Ayanda [47]2009NigeriaB. globosus3927218.377218.37S. haematobium7
B. pfeifferi2565220.315220.31S. mansoni
Ibikounlé et al. [19]2009BeninB. pfeifferi35720.5620.56S. mansoni8
Zongo et al. [20]2009Burkina FasoB. truncatus2727.4027.40S. haematobium7
Akinwale et al. [53]2011NigeriaB. truncatus1381384129.704129.70S. haematobium7
Lotf et al. [26]2011EgyptB. alexandrina277176.10176.10S. mansoni7
Mengistu et al. [34]2011EthiopiaBiomphalaria spp.56032558.0032558.00S. mansoni7
Opisa et al. [38]2011KenyaB. pfeifferi42571.6071.60S. mansoni9
B. sudanica40771.7071.70S. mansoni
B. globosus22752.2052.20S. haematobium
Abe et al. [50]2012NigeriaB. truncatus562544.642544.64S. haematobium7
Iboh et al. [48]2012NigeriaB. globosus1201310.801310.80S. haematobium8
Mekonnen et al. [35]2012EthiopiaB. pfeifferi8022.5022.50S. mansoni7
Kinanpara [23]2013Côte d’IvoireB. globosus1892312.172312.17S. haematobium7
B pfeifferi1409251.77251.77S. mansoni
Alebie et al. [31]2014EthiopiaB. pfeifferi3013210.603210.60S. mansoni7
Angelo et al. [62]2014TanzaniaB. sudanica1470110.75110.75S. mansoni8
Ivoke et al. [49]2014NigeriaB. globosus3086220.106220.10S. haematobium8
Moser et al. [22]2014ChadB. truncatus411910.8010.02S. haematobium8
B. pfeifferi10810.9010.90S, mansoni
Akinwale et al. [54]2015NigeriaB. globosus1091093834.803834.80S. haematobium9
B. forskalii2222836.40836.40S. haematobium
B. camerunensis77457.00457.00S. haematobium
B. senegalensis1111218.20218.20S. haematobium
Amsalu et al. [33]2015EthiopiaB. pfeifferi3113.2013.20S. mansoni7
Bado et al. [41]2015MaliB. truncatus324113.40113.40S. haematobium8
B. pfeifferi18921.1021.10S. mansoni
Gashaw et al. [32]2015EthiopiaB. pfeifferi14214.30214.30S. mansoni7
Rowel et al., [67]2015UgandaBiomphalaria spp193551270.701270.70S. mansoni9
Senghor [55]2015SenegalB. senegalensis733380.1180.11S. haematobium9
B. umbilicatus339226.51226.51S. haematobium
Aboelhadid et al. [27]2016EgyptB. alexandrina8222222.80222.68S. mansoni7
B. truncatus42392.1092.10S. haematobium
Farghaly et al. [28]2016EgyptB. alexandrina40030.8400133.3133.3S. mansoni9
Mohammed et al. [57]2016SudamB. truncatus140320.1020.10S. haematobium9
B. pfeifferi5100821.60821.60S. mansoni
Pennance [63]2016TanzaniaB. globosus1111262.30262.30S. haematobium8
Alemayehu et al. [36]2017EthiopiaB. pfeifferi11176.3076.30S. mansoni8
Allan et al. [18]2017AngolaB. globosus1732514.502514.50S. haematobium8
Bakuza et al. [69]2017TanzaniaB. pfeifferi2352912.3021910347.0010343.8S. mansoni8
Gouvras et al. [61]2017TanzaniaB. sudanica35,9104391.214391.21S. mansoni7
B. choanomphala6906610.88610.88S. mansoni
Okeke and Ubachukwu [52]2017NigeriaB. pfeifferi460204.30204.30S. mansoni8
Stanton et al. [65]2017UgandaBiomphalaria spp.49951.001182218.64275.4S. mansoni8
Aliyu et al. [51]2018NigeriaB. pfeifferi59215626.0015626.00S. mansoni8
B. truncatus5942142123.90142123.90S. haematobium
B. globosus8894216624.30216624.30S. haematobium
Afiukwa et al. [46]2019NigeriaB. globosus1773419.203419.20S. haematobium8
B. truncatus1061817.001817.00S. haematobium
Okeke et al. [45]2019NigeriaB. pfeifferi212--212167.45167.45S. mansoni8
Peletu et al. [44]2019NigeriaB. globosus11254.5054.50S. haematobium9
Rabone et al. [42]2019NigerB. forskalii11989240.20240.20S. haematobium9
B. pfeifferi2290793.40793.40S. mansoni
Tian-Bi et al. [24]2019Côte d’IvoireB. truncatus177220.1020.10S. haematobium9
B. globosus24752.0052.00S. haematobium
Catalano et al. [56]2020SenegalB. pfeifferi40792.2092.20S. mansoni7
Fuss et al. [59]2020TanzaniaB. sudanica78878827935.4027935.4S. mansoni9
Mutsaka-Makuvaza et al. [68]2020ZimbabweB. globosus1542301.90301.90S. haematobium9

3.3. Risk of Bias within Studies

The Newcastle–Ottawa quality assessment scale indicated that there was no bias within studies. The individual study included in this review was moderate to high-quality score as indicated in Table 1.

3.4. Prevalence of S. mansoni and S. haematobium Cercaria Among Freshwater Snails

A total of 273, 643 snails from Biomphalaria and Bulinus genera were examined for the presence of S. mansoni and S. haematobium cercaria in the 51 eligible studies, respectively (Table 2). Out of these snails, 8,682 of them were infected by either S. mansoni or S. haematobium. The prevalence of schistosome cercaria in the individual study ranged from 0.05% to 58.03% with substantial heterogeneity across studies within and across countries. The pooled prevalence of schistosome cercaria among freshwater snails was 5.5% (95% CI: 4.9–6.1%, I2 = 99.4%, and ) (Figure 2).


Snail genusSnail speciesStudies (n)Examined snails (n)Infected snails
npp (95%CI)

BiomphalariaB. pfeifferi19464809875.10 (4.05–6.15)
B. sudanica54702710326.73 (4.46–9.01)
B. alexandrina43569622.81 (0.75–4.87)
B. choanomphala216,1002251.58 (0.44–2.21)
B. stanleyi121,7159494.37 (4.09–4.64)
Unclassified Biomphalaria snails32041447921.28 (-1.78–44.34)

BulinusB. globosus1413691251112.25 (6.23–18.27)
B. truncatus134253820775.78 (4.36–7.20)
B. nasutus2286482780.98 (0.76–1.20)
B. senegalensis27344104.73 (-10.72–20.18)
B. umbilicatus1339226.49 (3.71–9.27)
B. forskalii321461370.13 (0.08–0.34)
B. camerunensis17457.14 (21.30–92.99)
Unclassified Bulinus snails1431292.1 (0.10–3.90)

Total51273 64386825.51 (4.95–6.07)

3.5. Subgroup Analysis

The highest pooled prevalence of schistosome cercaria was observed among freshwater snails from Nigeria (19.0%; 95% CI: 12.7–25.3%), followed by Ethiopia (15.9%; 95% CI: −5.9–37.5%), Mali (5.2%; 95% CI: -0.3–10.7%), and Tanzania (4.9%; 95% CI: 3.8–6.0%) (Figure 3). We categorized the years of studies into four groups: before 2000, 2001 to 2010, 2011 to 2015, and 2016 to June 2020 to assess the trends on the prevalence of schistosome cercaria in freshwater snails. The pooled prevalence of schistosome cercaria among freshwater snails in years before 2000, 2001–2010, 2011–2015, and 2016–2020 was 1.3% (95% CI: 0.8–1.8%), 2.8% (95% CI: 1.8–3.8%), 6.1% (95% CI: 5.2–7%), and 8.3% (95% CI: 6.6–9.9%), respectively, in Africa (Figure 4).

This meta-analysis targets the two most common and widely distributed Schistosoma species (S. mansoni and S. haematobium) in the continent. Biomphalaria and Bulinus snails were the intermediate hosts for S. mansoni and S. haematobium, respectively. The pooled prevalence of S. mansoni cercaria in Biomphalaria snails was 5.6% (95% CI: 4.9–6.3%) while the pooled prevalence of S. haematobium cercaria in Bulinus snails was 5.2% (95% CI: 4.7–5.7%) (Figure 5).

The pooled prevalence of S. mansoni and S. haematobium among freshwater snails was varied from country to country. The highest pooled prevalence of S. mansoni among Biomphalaria snails was observed from Tanzania (16.6%) followed by Ethiopia (15.9%) and Nigeria (14.5%) (Figure S1). On the contrary, the highest pooled prevalence of S. haematobium among Bulinus snail was observed from Nigeria (19.6%) followed by Angola (14.5%) and Côte d’Ivoire (9.6%) (Figure S2).

Twelve snail species from Biomphalaria and Bulinus snails were reported in the eligible articles used for this meta-analysis (Table 2). Among these species, Biomphalaria pfeifferi was the most common snail species and reported from 19 studies (37.3%) from the total 51 studies included in this study. The pooled prevalence of S. mansoni cercaria was 5.1% (95% CI: 4.1–6.2%) among B. pfeifferi snails. Bulinus snail, particularly B. globosus and B. truncatus, were the second and third most reported snails species (reported in 14 and 13 studies, respectively) that serve as an intermediate host for S. haematobium. The pooled prevalence of S. haematobium cercaria was 12.3% (95% CI: 6.2–18.3%) and 5.8% (95% CI: 4.4–7.2%) in B. globosus and B. truncatus snails, respectively (Table 2).

The studies included in this meta-analysis used shedding of cercariae and PCR-based detection of schistosomes from snail tissue. The pooled prevalence of schistosomes obtained by shedding of cercariae was 4.5% (95% CI: 3.9–5.1%) in contrast to 26.7% (95% CI: 10.5–43.0%) obtained by PCR techniques (Figure 6).

3.6. Publication Bias across Studies

The funnel plot symmetry demonstrates the presence of publication bias among studies included in this meta-analysis (Figure 7). Similarly, Egger’s test results () and Begg’s test () confirm the presence of publication bias among studies.

3.7. Metaregression Analysis and Sensitivity Test

There were clear heterogeneities across studies included in this meta-analysis. We performed a meta-regression analysis to identify the sources of heterogeneity across studies. The metaregression analysis showed that methods of schistosome detection from snails (regression coefficient: 2.55, 95% CI, 1.17–5.54, ) might be the source of heterogeneity. The country of study (regression coefficient: 0.99, 95% CI, 0.89–1.11, ), years of publication (regression coefficient: 1.41, 95% CI, 0.91–2.18, ), snail genus (regression coefficient: 1.19, 95% CI, 0.56–2.55, ), and snail species (regression coefficient: 0.92, 95% CI, 0.8 ) did not contribute for the heterogeneity. Besides, a sensitivity analysis was performed by recalculating the pooled prevalence by sequentially removing one-by-one to assess the effect of individual studies to overall effect. The pooled prevalence remained stable, and the result was not driven by individual studies included in the meta-analysis.

4. Discussion

Schistosomiasis is the second leading cause of infectious diseases next to malaria in Africa. Despite intensive efforts to tackle schistosomiasis, the prevalence is still unacceptably high in many African countries. The control and prevention strategies mainly rely on treatment of infected cases and mass drug administration of school-aged children. In many African countries, snail control strategies are not routinely implemented and sometimes considered as old-fashion approaches [70] despite their vital contributions to the elimination of schistosomes witnessed from Japan, Iran, and Tunisia [7173]. In addition, enormous progresses have been observed in the elimination program from Morocco, Oman, Lebanon, and Caribbean Islands [73, 74]. The intensity and prevalence of schistosomes’ infection among freshwater snails are scarce from many African countries. Summarized information about the prevalence of schistosomes among snail intermediate hosts is important for policymakers to give better attention to snail control strategies in Africa.

The overall pooled prevalence of schistosome cercaria was nearly 6% among freshwater snails in Africa. This finding is slightly lower than 9% reported from freshwater snails in Brazil [75]. In contrast, a lower prevalence of infected snails was observed from Indonesia [76] and Brazil [77]. These differences might be associated with prevalence and intensity of schistosome infection in the community, the level of environmental sanitation, suitability of the climate for the snails, level of existing snail control strategies, level of human exposure to open surface water, methods of schistosome detection, and seasons of snail collection and examination.

The highest pooled prevalence of schistosome cercaria among freshwater snails was observed in Nigeria followed by Ethiopia. In contrast, low prevalences of schistosomes were observed from Benin, Burundi, and Chad. The high prevalence of schistosomes among snail species in Nigeria and Ethiopia might be associated with the high prevalence of schistosomes in the community. The prevalence of schistosomiasis could reach as high as 90% in Ethiopia [78] and 94% in Nigeria [79, 80]. In addition, the difference in the level of environmental sanitation and the suitability of the area for the intermediate host, as well as the types of snail species in the area, may contribute for the difference in infection of snails across countries. Moreover, larger numbers of studies were reported from these two countries. Out of 51 studies, 17 (23.9%) studies included in this review were from the two countries.

Several species of freshwater snails that potentially serve as intermediate hosts for S. mansoni and S. haematobium have been recently reviewed [81]. Biomphalaria and Bulinus snails are the common and widely distributed intermediate hosts for schistosomes in Africa. The twelve snail species observed in this review belonged to either Biomphalaria or Bulinus genus.

Biomphalaria snails are well-known intermediate hosts of S. mansoni in Africa. This review showed that 5.6% of Biomphalaria snails were infected by S. mansoni in Africa. The highest pooled prevalence of S. mansoni was observed from Tanzania followed by Ethiopia and Nigeria, while low pooled prevalence was reported from Benin, Burundi, and Chad. These reported differences might be associated with the level of environmental sanitation, the abundance of Biomphalaria snails, and seasons of snail collection and examination. The highest prevalence of S. mansoni among Biomphalaria snails was reported during the dry season or just before the beginning of the rain seasons [47, 82].

Five species of Biomphalaria snails (B. pfeifferi, B. sudanica, B. choanomphala, B. alexandrina, and B. stanleyi) were included in the eligible articles for this review. As reviewed by Abe et al. [81], B. pfeifferi, B. sudanica, B. choanomphala, and B. alexandrina were the common intermediate hosts of S. mansoni in Africa. The pooled prevalence of S. mansoni varied from 1.3% to 6.7% among these snail species.

Biomphalaria pfeifferi were the most common snails infected by schistosome parasite. About 40% of the eligible studies included in this meta-analysis reported B. pfeifferi. The role of B. pfeifferi as an intermediate host of S. mansoni varied from country to country. Biomphalaria pfeifferi is the sole intermediate host for S. mansoni in Côte d’Ivoire [83] and Senegal [84] and the dominant intermediate host in many other African countries [8588].

Biomphalaria sudanica was the second common Biomphalaria snails that serve as an intermediate host for S. mansoni as observed in this study. Biomphalaria sudanica is an intermediate host for S. mansoni in Kenya [47] and Tanzania [19, 89]. Biomphalaria sudanica is also reported from Ethiopia but limited to around Lake Ziway [90] and Tikur Wuha [87].

Biomphalaria alexandrina was the third common intermediate host for S. mansoni observed in this study. However, its contribution as an intermediate host for S. mansoni is restricted in geographical distribution, mainly reported from Egypt [9193]. Biomphalaria choanomphala was another intermediate host for Schistosoma mansoni reported from Uganda [64] and Tanzania [61]. This snail species is widely distributed around Lake Victoria, which is divided among three countries (Kenya, Tanzania, and Uganda). Biomphalaria choanomphala is also reported from Kenya [94], but the infection intensity was not determined.

Bulinus snail is the common intermediate host for S. haematobium in Africa. This study revealed that about 5.2% of Bulinus snails were infected with S. haematobium in Africa. The highest pooled prevalence of S. haematobium infection among Bulinus snail was observed from Nigeria followed by Angola and Côte d’Ivoire. In contrast, there was a low prevalence of S. haematobium infection among Bulinus snails from Chad, Niger, Senegal, and Sudan. These variations might be associated with the difference in the level of endemicity of S. haematobium in the countries. A recent review indicated that about one-third of the populations of Nigeria were infected by S. haematobium [95, 96]. The higher infection intensity in the population might lead to a high level of environmental contamination that resulted in higher snail infection in Nigeria.

The eligible studies included in this review report seven species of Bulinus snails (B. truncates B. globosus, B. forskalii, B. senegalensis, B. nasutus, B. camerunensis, and B. umbilicatus) from African countries. According to Abe et al. [81], B. truncates, B. africanus, B. forskalii, B. senegalensis, and B. camerunensis were the predominant Bulinus snails that serve as an intermediate host for S. haematobium.

Among the Bulinus snails, B. globosus was reported from 14 studies in 7 African countries included in this review. The present study revealed that 12.3% of B. globosus was infected by S. haematobium. Similarly, high pooled prevalence (18%) of S. haematobium among B. globosus was recently reported in a meta-analysis from Nigeria [96]. Bulinus truncatus are the other important Bulinus snails that serve as an intermediate host for S. haematobium in Africa. The pooled prevalence of S. haematobium was 5.9% among Bulinus truncatus snails in Africa. In contrast to our result, 19% prevalence of S. haematobium was reported from B. truncates snails in Nigeria [31]. Similarly, B. truncatus is the predominant intermediate host for S. haematobium in Niger [42] and Côte d’Ivoire [23, 24].

Detection of schistosome infection is determined by shedding of cercariae and/or PCR based approaches from snail tissue. There was a significant difference in the pooled prevalence of schistosome results between shedding of cercaria (4.5%) and PCR (26.7%) among snail species in Africa. Similar differences (1.56% vs. 39.8%) are seen in the prevalence of schistosome infection between cercarial shedding and PCR methods among snails as reported from Kenya [97]. This difference is associated with the sensitivity of PCR to detect schistosome infection from snail tissue. Cercarial shedding is suffered by several limitations such as low parasite burden; snails may not shed cercariae during the prepatent period; time-consuming, and labour-intensive [98]. PCR-based detection of schistosome infection from snails is generally rapid, efficient, sensitive, and cost-effective for large-scale detection [99, 100].

Despite the ongoing schistosomiasis control strategies in many African countries, the pooled prevalence of schistosomes among freshwater snails had increased over time from 1.3% (before 2000) to 8.3% between 2016 and 2020. This might be attributed to the large number of epidemiological studies conducted and reported recently. Besides, molecular based detection of schistosome infection from snail tissue received attention in the recent years. These situations may contribute to the increased prevalence of schistosomes among freshwater snails recently.

4.1. Limitation of the Study

Although this systematic review generated valuable data on the prevalence of S. mansoni and S. haematobium among freshwater snails in Africa, it also has limitations. First, information on the prevalence of schistosome cercaria among snail species was not obtained from all African countries. Prevalence data were available only from 17 African countries. The pooled prevalences of schistosomes in this review may not fully represent the prevalence of S. mansoni and S. haematobium among freshwater snails of Africa. Second, the numbers of published studies were not evenly distributed even in the 17 countries (varied from 1 study to 11 studies in a country). Third, the studies included in this review were published in English, and we did not include studies published in other languages such as French due to language barriers and translation-related challenges. Fourth, most of the studies included in this review used cercarial shedding rather than PCR for the detection of schistosome infection. Cercarial shedding is less sensitive for the detection of schistosomes due to its inherent limitation that may result in low prevalence of schistosomes among infected snails in Africa. The pooled prevalence of schistosome cercaria among freshwater snails of Africa observed in this review might be below the actual infection intensity. Fifth, this review showed that there was high heterogeneity across studies included in this review. These might be associated with study design, seasons of snail collection, method of detection, and variation of endemicity of schistosomes across countries.

5. Conclusions

This review showed that nearly 6% of freshwater snails in Africa were infected by either S. haematobium or S. mansoni. The pooled prevalences of schistosome cercaria among freshwater snails have increased in the recent years in many African countries. The higher and increased trends in the prevalence of schistosomes among freshwater snails highlight the need for appropriate snail control strategies in the region. Policymakers should give better attention about integration of snail control strategies to the ongoing treatment-based prevention of schistosomiasis in Africa.

Abbreviations

CI:Confidence interval
I2:Inverse variance index
NOS:Newcastle–Ottawa quality assessment scale
PRISMA:Preferred Reporting Items for Systematic Reviews and Meta-analysis
PCR:Polymerase chain reaction
NTD:Neglected tropical disease.

Data Availability

All the datasets are included in the manuscript.

Conflicts of Interest

The authors declare that there are no conflicts of interest.

Authors’ Contributions

TH was involved in the design, conducted the review, data analysis, and interpretation of the findings, and drafted the manuscript. EN and AM were involved in drafting the manuscript, reviewing, and editing the manuscript.

Supplementary Materials

S1 Table: PRISMA checklist. S1 Text : NEWCASTLE–OTTAWA QUALITY ASSESSMENT SCALE. S1 Fig : forest plot showing the pooled effect estimate of S. mansoni among Biomphalaria snails in Africa. S2 Fig : forest plot showing the pooled prevalence estimate of S. haematobium among Bulinus snails in Africa. (Supplementary Materials)

References

  1. WHO, “Schistosomiasis,” 2020, https://www.who.int/news-room/fact-sheets/detail/schistosomiasis. View at: Google Scholar
  2. M. A. Barry, G. G. Simon, and N. Mistry, “Global trends in neglected tropical disease control and elimination: impact on child health,” Archives of Disease in Childhood, vol. 98, no. 8, p. 635, 2013. View at: Publisher Site | Google Scholar
  3. P. Hotez, J. Keiser, R. Bos, M. Tanner, and J. Utzinger, “Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk,” The Lancet Infectious Diseases, vol. 6, no. 7, pp. 411–425, 2006. View at: Publisher Site | Google Scholar
  4. M. T. Inobaya, R. M. Olveda, T. N. Chau, D. U. Olveda, and A. G. Ross, “Prevention and control of schistosomiasis: a current perspective,” Research and Reports in Tropical Medicine, vol. 2014, no. 5, pp. 65–75, 2014. View at: Google Scholar
  5. D. G. Colley, A. L. Bustinduy, W. E. Secor, and C. H. King, “Human schistosomiasis,” The Lancet, vol. 383, no. 9936, pp. 2253–2264, 2014. View at: Publisher Site | Google Scholar
  6. B. Gryseels, K. Polman, J. Clerinx, and L. Kestens, “Human schistosomiasis,” The Lancet, vol. 368, no. 9541, pp. 1106–1118, 2006. View at: Publisher Site | Google Scholar
  7. R. E. Blanton, “Population structure and dynamics of helminthic infection: schistosomiasis,” Microbiology spectrum, vol. 7, no. 4, 2019. View at: Publisher Site | Google Scholar
  8. A. Pinto-Almeida, T. Mendes, R. N. de Oliveira, S. A. P. Corrêa, S. M. Allegretti et al., “Morphological characteristics of Schistosoma mansoni PZQ-resistant and -susceptible strains are different in presence of praziquantel,” Frontier Microbiology, vol. 7, no. 594, 2016. View at: Publisher Site | Google Scholar
  9. J. A. Rozendaal, Vector Control: Methods for Use by Individuals and Communities: Freshwater Snails, WHO, Geneva, Switzerland, 1997.
  10. D. S. Brown, Freshwater Snails of Africa and Their Medical Importance, Tailers and Francis, London, UK, 1994.
  11. R. A. Kane, J. R. Stothard, A. M. Emery, and D. Rollinson, “Molecular characterization of freshwater snails in the genus Bulinus: a role for barcodes?” Parasites & Vectors, vol. 1, no. 1, p. 15, 2008. View at: Publisher Site | Google Scholar
  12. Q. P. Zhao, M. S. Jiang, D. T. J. Littlewood, and P. Nie, “Distinct genetic diversity of Oncomelania hupensis, intermediate host of Schistosoma japonicum in mainland China as revealed by ITS sequences,” PLoS Neglected Tropical Diseases, vol. 4, no. 3, p. e611, 2010. View at: Publisher Site | Google Scholar
  13. D. Moher, A. Liberati, J. Tetzlaff, and D. G. Altman, “Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement,” BMJ, vol. 339, 2009. View at: Publisher Site | Google Scholar
  14. G. A. Wells, B. Shea, D. O’Connell, J. Peterson, V. Welch et al., The Newcastle-Ottawa Scale (NOS) for Assessing the Quality of Nonrandomised Studies in Meta-Analyses, 2012, http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.
  15. A.-M. Lewis-Mikhael, A. Bueno-Cavanillas, T. Ofir Guiron, R. Olmedo-Requena, M. Delgado-Rodríguez, and J. J. Jiménez-Moleón, “Occupational exposure to pesticides and prostate cancer: a systematic review and meta-analysis,” Occupational and Environmental Medicine, vol. 73, no. 2, p. 134, 2016. View at: Publisher Site | Google Scholar
  16. J. P. T. Higgins, S. G. Thompson, J. J. Deeks, and D. G. Altman, “Measuring inconsistency in meta-analyses,” BMJ, vol. 327, no. 7414, pp. 557–560, 2003. View at: Publisher Site | Google Scholar
  17. W. G. Melsen, M. C. J. Bootsma, M. M. Rovers, and M. J. M. Bonten, “The effects of clinical and statistical heterogeneity on the predictive values of results from meta-analyses,” Clinical Microbiology and Infection, vol. 20, no. 2, pp. 123–129, 2014. View at: Publisher Site | Google Scholar
  18. F. Allan, J. C. Sousa-Figueiredo, A. M. Emery, R. Paulo, C. Mirante et al., “Mapping freshwater snails in north-western Angola: distribution, identity and molecular diversity of medically important taxa,” Parasites & Vectors, vol. 10, no. 1, p. 460, 2017. View at: Publisher Site | Google Scholar
  19. M. Ibikounlé, G. Mouahid, N. G. Sakiti, A. Massougbodji, and H. Moné, “Freshwater snail diversity in Benin (West Africa) with a focus on human schistosomiasis,” Acta Tropica, vol. 111, no. 1, pp. 29–34, 2009. View at: Publisher Site | Google Scholar
  20. D. Zongo, B. G. Kabre, D. Dianou, B. Savadogo, and J. N. Poda, “Importance of malacological factors in the transmission of Schistosoma haematobium in two dams in the province of oubritenga (burkina faso),” Research Journal of Environmental Sciences, vol. 3, no. 1, pp. 127–133, 2009. View at: Publisher Site | Google Scholar
  21. B. Gryseels, “The epidemiology of schistosomiasis in Burundi and its consequences for control,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 85, no. 5, pp. 626–633, 1991. View at: Publisher Site | Google Scholar
  22. W. Moser, H. Greter, C. Schindler et al., “The spatial and seasonal distribution of Bulinus truncatus, Bulinus forskalii and Biomphalaria pfeifferi, the intermediate host snails of schistosomiasis, in N’Djamena, Chad,” Geospatial Health, vol. 9, no. 1, pp. 109–118, 2014. View at: Publisher Site | Google Scholar
  23. K. Kinanpara, B. K. Yves, K. K. Félix, E. O. Edia, G. Théophile et al., “Freshwater snail dynamics focused on potential risk of using urine as fertilizer in Katiola, an endemic area of schistosomiasis (ivory coast; West Africa),” Journal of Entomology and Zoology Studies, vol. 1, no. 5, pp. 110-111, 2013. View at: Google Scholar
  24. Y.-N. T. Tian-Bi, B. Webster, C. K. Konan, F. Allan, N. R. Diakité et al., “Molecular characterization and distribution of Schistosoma cercariae collected from naturally infected bulinid snails in northern and central Côte d’Ivoire,” Parasites & Vectors, vol. 12, no. 1, p. 117, 2019. View at: Publisher Site | Google Scholar
  25. A.-N. A. Hussein and S. M. Bin-Dajem, “Prevalence of urinary schistosomiasis and Infections withTrematode larval stages in Bulinus truncatus snails from Qena Upper Egypt,” Journal of Applied Sciences Research, vol. 4, no. 11, pp. 1610–1617, 2008. View at: Google Scholar
  26. W. M. Lotfy, B. Hanelt, G. M. Mkoji, and E. S. Loker, “Genotyping natural infections of Schistosoma mansoni in Biomphalaria alexandrina from damietta, Egypt, with comparisons to natural snail infections from Kenya,” Journal of Parasitology, vol. 97, no. 1, pp. 156–159, 2011. View at: Publisher Site | Google Scholar
  27. S. M. Aboelhadid, M. Thabet, D. El-Basel, and R. Taha, “Digenetic larvae in Schistosome snails from El Fayoum, Egypt with detection of Schistosoma mansoni in the snail by PCR,” Journal of Parasitic Diseases, vol. 40, no. 3, pp. 730–734, 2016. View at: Publisher Site | Google Scholar
  28. A. Farghaly, A. A. Saleh, S. Mahdy et al., “Molecular approach for detecting early prepatent Schistosoma mansoni infection in Biomphalaria alexandrina snail host,” Journal of Parasitic Diseases, vol. 40, no. 3, pp. 805–812, 2016. View at: Publisher Site | Google Scholar
  29. A.-N. A. Hussein and S. A. H. Rabie, “Schistosoma mansoni and trematode larval stages in Biomphalaria alexandrina in Qena Governorate, Egypt,” Journal of the Egyptian-German Society of Zoology, vol. 53, pp. 1–15, 2007. View at: Google Scholar
  30. C. L. King, R. Barkat, A. S. Monto, F. D. Miller, and M. Hussein, “Prevalence and intensity of schistosoma haematobium infection in six villages of upper Egypt,” The American Journal of Tropical Medicine and Hygiene, vol. 31, no. 2, pp. 320–327, 1982. View at: Publisher Site | Google Scholar
  31. G. Alebie, B. Erko, M. Aemero, and B. Petros, “Epidemiological study on Schistosoma mansoni infection in sanja area, Amhara region, Ethiopia,” Parasites & Vectors, vol. 7, no. 1, p. 15, 2014. View at: Publisher Site | Google Scholar
  32. F. Gashaw, M. Aemero, M. Legesse, B. Petros, T. Teklehaimanot et al., “Prevalence of intestinal helminth infection among school children in maksegnit and enfranz towns, northwestern Ethiopia, with emphasis on Schistosoma mansoni infection,” Parasites & Vectors, vol. 8, no. 1, p. 567, 2015. View at: Publisher Site | Google Scholar
  33. G. Amsalu, Z. Mekonnen, and B. Erko, “A new focus of schistosomiasis mansoni in Hayk town, northeastern Ethiopia,” BMC Research Notes, vol. 8, no. 1, p. 22, 2015. View at: Publisher Site | Google Scholar
  34. M. Mengistu, T. Shimelis, W. Torben, A. Terefe, T. Kassa et al., “Human intestinal Schistosomiasis in communities living near three rivers of Jimma town, south western Ethiopia,” Journal of Health Science Research, vol. 21, no. 2, pp. 111–118, 2011. View at: Publisher Site | Google Scholar
  35. Z. Mekonnen, H. Haileselassie, G. Medhin, B. Erko, and N. Berhe, “Schistosomia mansoni focus in Mekele city, northern Ethiopia,” Ethiopian Medical Journal, vol. 50, no. 4, pp. 331–336, 2012. View at: Google Scholar
  36. B. Alemayehu, Z. Tomass, F. Wadilo, D. Leja, S. Liang et al., “Epidemiology of intestinal helminthiasis among school children with emphasis on Schistosoma mansoni infection in Wolaita zone, Southern Ethiopia,” BMC Public Health, vol. 17, p. 587, 2017. View at: Publisher Site | Google Scholar
  37. H. C. Kariuki, E. M. Muchiri, J. A. Clennon et al., “Distribution patterns and cercarial shedding of Bulinus nasutus and other snails in the Msambweni area, coast province, Kenya,” The American Journal of Tropical Medicine and Hygiene, vol. 70, no. 4, pp. 449–456, 2004. View at: Publisher Site | Google Scholar
  38. S. Opisa, M. R. Odiere, W. G. Jura, D. M. Karanja, and P. N. Mwinzi, “Malacological survey and geographical distribution of vector snails for schistosomiasis within informal settlements of Kisumu City, western Kenya,” Parasites & Vectors, vol. 4, no. 1, p. 226, 2011. View at: Publisher Site | Google Scholar
  39. R. F. Sturrock, S. J. Karamsadkar, and J. Ouma, “Schistosome infection rates in field snails:Schistosoma mansoniin Biomphalaria pfeifferi from Kenya,” Annals of Tropical Medicine & Parasitology, vol. 73, no. 4, pp. 369–375, 1979. View at: Publisher Site | Google Scholar
  40. A. Dabo, P. Durand, S. Morand et al., “Distribution and genetic diversity of Schistosoma haematobium within its bulinid intermediate hosts in Mali,” Acta Tropica, vol. 66, no. 1, pp. 15–26, 1997. View at: Publisher Site | Google Scholar
  41. A. Dabo, A. Z. Diarra, V. Machault, O. Touré, D. S. Niambélé et al., “Urban schistosomiasis and associated determinant factors among school children in Bamako, Mali, West Africa,” Infectious Diseases of Poverty, vol. 4, no. 1, p. 4, 2015. View at: Publisher Site | Google Scholar
  42. M. Rabone, J. H. Wiethase, F. Allan, A. N. Gouvras, T. Pennance et al., “Freshwater snails of biomedical importance in the Niger River Valley: evidence of temporal and spatial patterns in abundance, distribution and infection with Schistosoma spp,” Parasites & Vectors, vol. 12, no. 1, p. 498, 2019. View at: Publisher Site | Google Scholar
  43. R. Labbo, A. Djibrilla, H. Zamanka, A. Garba, and J.-P. Chippaux, “Bulinus forskalii: a new potential intermediate host for Schistosoma haematobium in Niger,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 101, no. 8, pp. 847-848, 2007. View at: Publisher Site | Google Scholar
  44. B. J. Peletu, I. E. Ofoezie, and R. F. Olaniyan, “Prevalence of fresh water snails transmitting Schistosoma haematobium in aponmu-lona river basin, idanre, ondo state, Nigeria,” International Journal of Marine Biology and Research, vol. 4, no. 1, pp. 1–7, 2019. View at: Google Scholar
  45. O. C. Okeke, O. P. Akinwale, P. O. Ubachukwu, P. V. Gyang, E. U. Henry et al., “Report of high prevalence of schistosome infection in Biomphalaria snails from a geographic area with no previous prevalence of human schistosomiasis in Nigeria,” Acta Tropica, vol. 210, Article ID 105326, 2019. View at: Google Scholar
  46. F. N. Afiukwa, D. E. Nwele, O. E. Uguru, G. A. Ibiam, C. S. Onwe et al., “Transmission dynamics of urogenital schistosomiasis in the rural community of ebonyi state, south eastern Nigeria,” Journal of Parasitology Research, vol. 2019, Article ID 7596069, 8 pages, 2019. View at: Publisher Site | Google Scholar
  47. O. I. Ayanda, “Prevalence of snail vectors of schistosomiasis and their infection rates in two localities within Ahmadu Bello University (A.B.U.) Campus, Zaria, Kaduna State, Nigeria,” Journal of Cell and Animal Biology, vol. 3, no. 4, pp. 58–61, 2009. View at: Google Scholar
  48. C. I. Iboh, O. N. Okon, S. E. Etim, I. E. Ukpong, E. I. Ognan et al., “Urinary schistosomiasis among kindergarten and primary school children in Okpechi community, cross river state, Nigeria: a preliminary study,” Journal of Engineering Science and Technology, vol. 1, no. 2, pp. 23–27, 2012. View at: Google Scholar
  49. 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. View at: Google Scholar
  50. E. M. Abe, A. S. Oluwole, D. A. Ojo, O. A. Idowu, C. F. Mafiana et al., “Predicting the geo-spatial distribution of Bulinus snail vector of urinary schistosomiasis in Abeokuta, South Western Nigeria,” The Zoologist, vol. 10, pp. 53–60, 2012. View at: Google Scholar
  51. I. W. Aliyu, P. S. Mao, and S. I. Danladi, “Transmission patterns among freshwater snail hosts of schistosomiasis in Bauchi area of Nigeria,” GSC Biological and Pharmaceutical Sciences, vol. 2, no. 2, pp. 18–24, 2018. View at: Google Scholar
  52. O. C. Okeke and P. O. Ubachukwu, “Trematode infections of the freshwater snail Biomphalaria pfeifferi from a south-east Nigerian community with emphasis on cercariae of Schistosoma,” Journal of Helminthology, vol. 91, no. 3, pp. 295–301, 2017. View at: Publisher Site | Google Scholar
  53. O. P. Akinwale, R. A. Kane, D. Rollinson et al., “Molecular approaches to the identification ofBulinusspecies in south-west Nigeria and observations on natural snail infections with schistosomes,” Journal of Helminthology, vol. 85, no. 3, pp. 283–293, 2011. View at: Publisher Site | Google Scholar
  54. O. Akinwale, O. Oso, O. Salawu et al., “Molecular characterisation of Bulinus snails-intermediate hosts of schistosomes in Ogun State, South-western Nigeria,” Folia Malacologica, vol. 23, no. 2, pp. 137–147, 2015. View at: Publisher Site | Google Scholar
  55. B. Senghor, O. T. Diaw, S. Doucoure, M. Seye, I. Talla et al., “Study of the snail intermediate hosts of urogenital schistosomiasis in Niakhar, region of Fatick, West central Senegal,” Parasites & Vectors, vol. 8, no. 1, p. 410, 2015. View at: Publisher Site | Google Scholar
  56. S. Catalano, E. Léger, C. B. Fall, B. Anna, S. D. Diop et al., “Multihost transmission of Schistosoma mansoni in Senegal, 2015–2018,” Emerging Infectious Diseases, no. 6, p. 26, 2020. View at: Google Scholar
  57. N. A. I. Mohammed, H. Madsen, and A. A. A. R. M. Ahmed, “Types of trematodes infecting freshwater snails found in irrigation canals in the East Nile locality, Khartoum, Sudan,” Infectious Diseases of Poverty, vol. 5, no. 1, p. 16, 2016. View at: Publisher Site | Google Scholar
  58. A. Getaneh, A. Ashenafi, and Y. Zerihun, “Current status of intestinal parasitic infections and associated factors among primary school children in Birbir town, Southern Ethiopia,” BMC Infectious Diseases, vol. 19, no. 1, p. 270, 2019. View at: Google Scholar
  59. A. Fuss, H. D. Mazigo, and A. Mueller, “Malacological survey to identify transmission sites for intestinal schistosomiasis on Ijinga Island, Mwanza, north-western Tanzania,” Acta Tropica, vol. 203, Article ID 105289, 2020. View at: Publisher Site | Google Scholar
  60. N. J. S. Lwambo, “Transmission of urinary schistosomiasis in Sukumaland, Tanzania. 1 snail infection rates and incidence of infection in school children,” Journal of Helminthology, vol. 62, no. 3, pp. 213–217, 1988. View at: Publisher Site | Google Scholar
  61. A. N. Gouvras, F. Allan, S. Kinung’hi, M. Rabone, A. Emery et al., “Longitudinal survey on the distribution of Biomphalaria sudanica and B. choanomophala in Mwanza region, on the shores of Lake Victoria, Tanzania: implications for schistosomiasis transmission and control,” Parasites & Vectors, vol. 10, no. 1, p. 316, 2017. View at: Publisher Site | Google Scholar
  62. T. Angelo, F. Shahada, A. Kassuku, H. Mazigo, C. Kariuki et al., “Population abundance and disease transmission potential of snail intermediate hosts of human schistosomiasis in fishing communities of Mwanza region, North-western Tanzania,” International Journal of Science and Research, vol. 3, no. 8, pp. 1230–1236, 2014. View at: Google Scholar
  63. T. Pennance, B. Person, M. A. Muhsin, A. N. Khamis, J. Muhsin et al., “Urogenital schistosomiasis transmission on Unguja Island, Zanzibar: characterisation of persistent hot-spots,” Parasites & Vectors, vol. 9, no. 1, p. 646, 2016. View at: Publisher Site | Google Scholar
  64. E. I. Odongo-Aginya, F. K. Kironde, N. B. Kabatereine, P. Kategere, and F. Kazibwe, “Effect of seasonal rainfall and other environmental changes, on snail density and infection rates with Schistosoma mansoni fifteen years after the last snails' study in Kigungu, Entebbe, Uganda,” East African medical journal, vol. 85, no. 11, pp. 556–563, 2008. View at: Google Scholar
  65. M. C. Stanton, M. Adriko, M. Arinaitwe, A. Howell, J. Davies et al., “Intestinal schistosomiasis in Uganda at high altitude (>1400 m): malacological and epidemiological surveys on mount elgon and in fort portal crater lakes reveal extra preventive chemotherapy needs,” Infectious Diseases of Poverty Journal, vol. 6, no. 1, p. 34, 2017. View at: Publisher Site | Google Scholar
  66. F. Kazibwe, B. Makanga, C. Rubaire-Akiiki et al., “Ecology of Biomphalaria (Gastropoda: Planorbidae) in Lake Albert, Western Uganda: snail distributions, infection with schistosomes and temporal associations with environmental dynamics,” Hydrobiologia, vol. 568, no. 1, pp. 433–444, 2006. View at: Publisher Site | Google Scholar
  67. C. Rowel, B. Fred, M. Betson, J. C. Sousa-Figueiredo, N. B. Kabatereine et al., “Environmental epidemiology of intestinal schistosomiasis in Uganda: population dynamics of Biomphalaria (gastropoda: Planorbidae) in lake albert and Lake Victoria with observations on natural infections with digenetic trematodes,” BioMed Research International, vol. 2015, Article ID 717261, 11 pages, 2015. View at: Publisher Site | Google Scholar
  68. M. J. Mutsaka-Makuvaza, X.-N. Zhou, C. Tshuma, E. Abe, J. Manasa et al., “Molecular diversity of Bulinus species in Madziwa area, Shamva district in Zimbabwe: implications for urogenital schistosomiasis transmission,” Parasites & Vectors, vol. 13, no. 1, p. 14, 2020. View at: Publisher Site | Google Scholar
  69. J. S. Bakuza, R. Gillespie, G. Nkwengulila et al., “Assessing S. mansoni prevalence in Biomphalaria snails in the Gombe ecosystem of western Tanzania: the importance of DNA sequence data for clarifying species identification,” Parasites and Vectors, vol. 10, no. 584, 2017. View at: Publisher Site | Google Scholar
  70. S. H. Sokolow, C. L. Wood, I. J. Jones et al., “To reduce the global burden of human schistosomiasis, use 'old fashioned' snail control,” Trends in Parasitology, vol. 34, no. 1, pp. 23–40, 2018. View at: Publisher Site | Google Scholar
  71. H. Tanaka and M. Tsuji, “From discovery to eradication of schistosomiasis in Japan: 1847-1996,” International Journal for Parasitology, vol. 27, no. 12, pp. 1465–1480, 1997. View at: Publisher Site | Google Scholar
  72. J. Utzinger, G. Raso, S. Brooker et al., “Schistosomiasis and neglected tropical diseases: towards integrated and sustainable control and a word of caution,” Parasitology, vol. 136, no. 13, pp. 1859–1874, 2009. View at: Publisher Site | Google Scholar
  73. A. F. Adenowo, B. E. Oyinloye, B. I. Ogunyinka, and A. P. Kappo, “Impact of human schistosomiasis in sub-Saharan Africa,” The Brazilian Journal of Infectious Diseases, vol. 19, no. 2, pp. 196–205, 2015. View at: Publisher Site | Google Scholar
  74. R. Barakat, H. El Morshedy, and A. Farghaly, “Human schistosomiasis in the Middle East and north Africa region,” in Neglected Tropical Diseases - Middle East and North Africa, M. A. McDowell and S. Rafati, Eds., pp. 23–57, Springer, Vienna, Austria, 2014. View at: Google Scholar
  75. T. A. S. Calasans, G. T. R. Souza, C. M. Melo, R. R. Madi, and V. S. Jeraldo, “Socioenvironmental factors associated with Schistosoma mansoni infection and intermediate hosts in an urban area of northeastern Brazil,” PLoS One, vol. 13, no. 5, Article ID e0195519, 2018. View at: Publisher Site | Google Scholar
  76. F. Satrija, Y. Ridwan, S. Jastal, A. Samarang, and A. Rauf, “Current status of schistosomiasis in Indonesia,” Acta Tropica, vol. 141, pp. 349–353, 2015. View at: Publisher Site | Google Scholar
  77. J. Gandasegui, P. Fernández-Soto, A. Muro, C. Simões Barbosa, F. Lopes de Melo et al., “A field survey using LAMP assay for detection of Schistosoma mansoni in a low-transmission area of schistosomiasis in Umbuzeiro, Brazil: assessment in human and snail samples,” PLoS Neglected Tropical Diseases, vol. 12, no. 3, Article ID e0006314, 2018. View at: Publisher Site | Google Scholar
  78. L. Worku, D. Damte, M. Endris, H. Tesfa, and M. Aemero, “Schistosoma mansoni infection and associated determinant factors among school children in sanja town, northwest Ethiopia,” Journal of Parasitology Research, vol. 2014, p. 7, 2014. View at: Publisher Site | Google Scholar
  79. O. P. Akinwale, M. B. Ajayi, D. O. Akande, M. A. Adeleke, P. V. Gyang et al., “Prevalence of Schistosoma haematobium infection in a neglected community, south western Nigeria,” International Healthcare Research Journal, vol. 2, no. 2, pp. 149–155, 2009. View at: Google Scholar
  80. C. O. Ezeh, K. C. Onyekwelu, O. P. Akinwale, L. Shan, and H. Wei, “Urinary schistosomiasis in Nigeria: a 50 year review of prevalence, distribution and disease burden,” Parasite, vol. 26, p. 19, 2019. View at: Publisher Site | Google Scholar
  81. E. M. Abe, W. Guan, Y.-H. Guo, K. Kassegne, Z.-Q. Qin et al., “Differentiating snail intermediate hosts of Schistosoma spp. using molecular approaches: fundamental to successful integrated control mechanism in Africa,” Infectious Diseases of Poverty, vol. 7, no. 1, p. 29, 2018. View at: Publisher Site | Google Scholar
  82. E. Dennis, P. Vorkpor, B. Holzer et al., “Studies on the epidemiology of schistosomiasis in Liberia: the prevalence and intensity of schistosomal infections in Bong County and the bionomics of the snail intermediate hosts,” Acta Tropica, vol. 40, no. 3, pp. 205–229, 1983. View at: Google Scholar
  83. N. R. Diakité, M. S. Winkler, J. T. Coulibaly, N. Guindo-Coulibaly, J. Utzinger et al., “Dynamics of freshwater snails and Schistosoma infection prevalence in schoolchildren during the construction and operation of a multipurpose dam in central Côte d’Ivoire,” Infectious Diseases of Poverty, vol. 6, no. 1, p. 93, 2017. View at: Publisher Site | Google Scholar
  84. M. Picquet, J. C. Ernould, J. Vercruysse et al., “The epidemiology of human schistosomiasis in the Senegal river basin,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 90, no. 4, pp. 340–346, 1996. View at: Publisher Site | Google Scholar
  85. K. Kock, C. Wolmarans, and M. Bornman, “Distribution and habitats of Biomphalaria pfeifferi, snail intermediate host of Schistosoma mansoni, in South Africa,” Water SA, vol. 30, no. 1, pp. 29–36, 2004. View at: Google Scholar
  86. A. C. Kengne-Fokam, H. C. Nana-Djeunga, M. Bagayan, and F. Njiokou, “Biomphalaria camerunensis as a viable alternative intermediate host for Schistosoma mansoni in southern Cameroon,” Parasites & Vectors, vol. 11, no. 1, p. 181, 2018. View at: Publisher Site | Google Scholar
  87. H. Mitiku, M. Legesse, Z. Teklemariam, and B. Erko, “Transmission of Schistosoma mansoni in tikur wuha area, southern Ethiopia,” The Ethiopian Journal of Health Development, vol. 24, no. 3, pp. 180–184, 2011. View at: Publisher Site | Google Scholar
  88. M. W. Mutuku, L. Lu, F. O. Otiato et al., “A comparison of Kenyan Biomphalaria pfeifferi and B. Sudanica as vectors for Schistosoma mansoni, including a discussion of the need to better understand the effects of snail breeding systems on transmission,” Journal of Parasitology, vol. 103, no. 6, pp. 669–676, 2017. View at: Publisher Site | Google Scholar
  89. A. F. Gabrielli, M. Ramsan, C. Naumann et al., “Soil-transmitted helminths and haemoglobin status among Afghan children in world food programme assisted schools,” Journal of Helminthology, vol. 79, no. 4, pp. 381–384, 2005. View at: Publisher Site | Google Scholar
  90. B. Erko, F. Balcha, and D. Kifle, “The ecology of Biomphalaria sudanica in Lake Ziway, Ethiopia,” African Journal of Ecology, vol. 44, no. 3, pp. 347–352, 2006. View at: Publisher Site | Google Scholar
  91. I. F. Abou-El-Naga, “Biomphalaria alexandrina in Egypt: past, present and future,” Journal of Biosciences, vol. 38, no. 3, pp. 665–672, 2013. View at: Publisher Site | Google Scholar
  92. S. M. F. El-Nassery, I. F. Abou-El-Naga, S. R. Allam, E. A. Shaat, and R. F. M. Mady, “Genetic variation between Biomphalaria alexandrina snails susceptible and resistant to schistosoma mansoni infection,” BioMed Research International, p. 160320, 2013. View at: Google Scholar
  93. T. A. Mansour, M. R. Habib, L. C. V. Rodríguez, A. H. Vázquez, J. M. Alers et al., “Central nervous system transcriptome of Biomphalaria alexandrina, an intermediate host for schistosomiasis,” BMC Research Notes, vol. 10, no. 1, p. 729, 2017. View at: Publisher Site | Google Scholar
  94. S. M. Bandoni, M. Mulvey, and E. S. Loker, “Population structure and taxonomic discrimination among three species of Biomphalaria preston, 1910 (Gastropoda: Planorbidae) from Kenya,” Zoological Journal of the Linnean Society, vol. 129, no. 3, pp. 387–401, 2000. View at: Publisher Site | Google Scholar
  95. A. Abdulkadir, M. Ahmed, B. M. Abubakar et al., “Prevalence of urinary schistosomiasis in Nigeria, 1994-2015: systematic review and meta-analysis,” African Journal of Urology, vol. 23, no. 3, pp. 228–239, 2017. View at: Publisher Site | Google Scholar
  96. P. O. Odeniran, K. F. Omolabi, and I. O. Ademola, “Epidemiological dynamics and associated risk factors of S. haematobium in humans and its snail vectors in Nigeria: a meta-analysis (1983-2018),” Pathogens and Global Health, vol. 114, no. 2, pp. 76–90, 2020. View at: Publisher Site | Google Scholar
  97. J. Hamburger, O. Hoffman, H. C. Kariuki et al., “Large-scale, polymerase Chain reaction-based surveillance of schistosoma haematobium dna in snails from transmission sites in coastal Kenya: a new tool for studying the dynamics of snail infection,” The American Journal of Tropical Medicine and Hygiene, vol. 71, no. 6, pp. 765–773, 2004. View at: Publisher Site | Google Scholar
  98. F. G. Abath, A. L. d. V. Gomes, F. L. Melo, C. S. Barbosa, and R. P. Werkhauser, “Molecular approaches for the detection of Schistosoma mansoni: possible applications in the detection of snail infection, monitoring of transmission sites, and diagnosis of human infection,” Memórias Do Instituto Oswaldo Cruz, Rio de Janeiro, Brazil, vol. 101, no. 1, pp. 145–148, 2006. View at: Publisher Site | Google Scholar
  99. R. L. Caldeira, L. K. Jannotti-Passos, and O. Dos Santos Carvalho, “Use of molecular methods for the rapid mass detection of Schistosoma mansoni (Platyhelminthes: trematoda) in Biomphalaria spp. (gastropoda: Planorbidae),” Journal of Tropical Medicine, vol. 2017, Article ID 8628971, 6 pages, 2017. View at: Publisher Site | Google Scholar
  100. J. Gandasegui, P. Fernández-Soto, J. Hernández-Goenaga, J. López-Abán, B. Vicente et al., “Biompha-LAMP: a new rapid loop-mediated isothermal amplification assay for detecting Schistosoma mansoni in Biomphalaria glabrata snail host,” PLoS Negl Trop Dis, vol. 10, no. 12, Article ID e0005225, 2016. View at: Publisher Site | Google Scholar

Copyright © 2020 Tamirat Hailegebriel 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.


More related articles

 PDF Download Citation Citation
 Download other formatsMore
 Order printed copiesOrder
Views2598
Downloads848
Citations

Related articles

Article of the Year Award: Outstanding research contributions of 2020, as selected by our Chief Editors. Read the winning articles.