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Bulinus Globosus Manyangadze et al. Parasites Vectors (2021) 14:222 https://doi.org/10.1186/s13071-021-04720-7 Parasites & Vectors RESEARCH Open Access Spatial and seasonal distribution of Bulinus globosus and Biomphalaria pfeiferi in Ingwavuma, uMkhanyakude district, KwaZulu-Natal, South Africa: Implications for schistosomiasis transmission at micro-geographical scale Tawanda Manyangadze1,2*, Moses John Chimbari1, Owen Rubaba1, White Soko1,3 and Samson Mukaratirwa4,5 Abstract Background: Schsistosomiasis is endemic in sub-Saharan Africa. It is transmitted by intermediate host snails such as Bulinus and Biomphalaria. An understanding of the abundance and distribution of snail vectors is important in design- ing control strategies. This study describes the spatial and seasonal variation of B. globosus and Bio. pfeiferi and their schistosome infection rates between May 2014 and May 2015 in Ingwavuma, uMkhanyakude district, KwaZulu-Natal province, South Africa. Methods: Snail sampling was done on 16 sites once every month by two people for 30 min at each site using the scooping and handpicking methods. Snails collected from each site were screened for schistosome mammalian cercariae by the shedding method. The negative binomial generalised linear mixed model (glmm) was used to deter- mine the relationship between abundances of the intermediate host snails and climatic factors [rainfall, land surface temperatures (LST), seasons, habitats, sampling sites and water physico-chemical parameters including pH and dis- solved oxygen (DO)]. Results: In total, 1846 schistosomiasis intermediate host snails were collected during the study period. Biompha- ria pfeiferi was more abundant (53.36%, n 985) compared to B. globosus (46.64%, n 861). Bulinus globosus was recorded at 12 sites (75%) and Bio. pfeiferi =was present at 7 sites (43.8%). Biompharia pfeiferi= cohabited with B. globo- sus at all the sites it was present. High numbers of Bio. pfeiferi (n 872, 88.5%) and B. globosus (n 705, 81.9%) were found between winter and mid-spring. Monthly rainfall showed =a statistically signifcant negative= relationship with the abundance of B. globosus (p < 0.05). Dissolved oxygen (DO) had a statistically signifcant positive relationship with the abundance of Bio. pfeiferi (p < 0.05) while (LST) had a statistically signifcant negative relationship (p < 0.05). More B. globosus (8.9%, n 861) were shedding schistosome mammalian cercariae compared to Bio. pfeiferi (0.1%, n 985) confrming the already= documented high prevalence of S. haematobium in Ingwavuma compared to S. mansoni=. *Correspondence: [email protected] 1 School of Nursing and Public Health, Department of Public Health Medicine, University of KwaZulu-Natal, Durban, South Africa Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Manyangadze et al. Parasites Vectors (2021) 14:222 Page 2 of 9 Conclusion: Results of this study provide updated information on the distribution of schistosomiasis intermediate host snails in the study area and contributes towards the understanding of the transmission dynamics of schistoso- miasis at the micro-geographical scale in this area. Keywords: Bulinus globosus, Biomphalaria pfeiferi, Schistosoma haematobium, Schistosoma mansoni, Malacology, Ecology Background Te aim of this study was to describe and analyse the Schistosoma haematobium and Schistosoma mansoni spatial and seasonal variation of B. globosus and Bio. are endemic in sub-Saharan Africa [1, 2] where they are pfeiferi in relation to a set of ecological factors at a mainly transmitted by Bulinus globosus and Biompha- micro-geographical scale in Ingwavuma of uMkhan- laria pfeiferi, respectively [3, 4]. Te transmission and yakude district, KwaZulu-Natal province, South Africa. focal distribution of schistosomiasis are spatially and Sound knowledge of the abundance and distribution of temporally restricted to water bodies inhabited by its intermediate host snails is key to understanding schisto- obligate intermediate host snails [1] and human water somiasis transmission in order to design efective inter- contact [5]. Schistosomiasis is a serious public health vention strategies in endemic areas [9]. problem in South Africa. An estimated 2–3 million children are infected, and 20 million (nearly 40% of the Methods population) are at risk [6]. Previous studies conducted in Study area Ingwavuma of uMkhanyakude district of South Africa Te study was conducted in Ingwavuma (Fig. 1) of uMkh- showed that the prevalence of S. haematobium was anyakude Health District in KwaZulu-Natal (KZN) prov- around 37.5% [7]. ince, South Africa, between May 2014 and May 2015. Te density and abundance of the intermediate host uMkhanyakude district is located in the northernmost snails for schistosomiasis are infuenced by environmen- eastern part of KwaZulu-Natal province of South Africa tal and climatic factors. Environmental factors include bordering Mozambique and Swaziland to the north and physical and chemical water properties such as tempera- northwest respectively. Te climate ranges from tropi- ture, turbidity, salinity, conductivity, pH and velocity and cal to subtropical [18] with a hot wet summer and a cold biological factors such as the availability of food, compe- dry winter. uMkhanyakude experiences low annual rain- tition, predator-prey interactions, presence and density fall averaging 690 mm per year. More than half of the of aquatic plants [1, 5, 8–10]. Rainfall and temperature households in this area do not have access to piped clean have been reported as the main climatic factors that water and have poor sanitary facilities [19, 20] making determine the distribution of intermediate host snails [4, them vulnerable to water-borne diseases (WBDs) includ- 11, 12]. ing schistosomiasis. Te study area is approximately Although the afore-mentioned factors have been well 40 × 30 km and mostly characterised by seasonal streams studied, their importance varies from one ecological zone fowing towards the Pongola food plain and two main to another and even from one water body to another in rivers (Pongolo and Ngwavuma) and there are two major the same ecological zone. Te ecological factors infuence dams—Nsunduza and Namaneni (Fig. 1). the presence and abundance of intermediate host snails [13]. Tus, it is important to conduct studies at a local Surveys for schistosomiasis vector snails scale to identify factors that are signifcant in particular Bulinus globosus and Bio. pfeiferi snails were sampled habitats to understand the schistosomiasis transmis- from 16 sites distributed across the whole study area sion dynamics [14]. Information on the ecology, tempo- (Fig. 1) every month from May 2014 to May 2015. Sam- ral distribution and population dynamics of B. globosus pling sites (including streams and dams) were identi- and Bio. pfeiferi at a local scale is needed to enhance the fed based on observations on human water contact [21] knowledge of the spatial and seasonal distribution and and following Appleton and Miranda’s [6] advice that factors infuencing these patterns [11]. Tis provides snails need to be collected from suspected transmis- critical data for the development and optimization of sion sites and screened for infection for the purposes control and management of the disease [15]. Although of local schistosomiasis surveillance. Twelve of the sites much work has been done to unravel the limiting factors were located at pools along the seasonal streams and 4 for snail habitat preferences [11, 12, 16], it is important to sites were located at dams to capture the spatial varia- gather data at a micro-geographical scale to understand tion in snail population dynamics at human water con- the local transmission dynamics [11, 16, 17]. tact patterns and diferent habitats. Te snail sampling Manyangadze et al. Parasites Vectors (2021) 14:222 Page 3 of 9 Fig. 1 Study area and snail sampling sites (indicated by red star) in Ingwavuma (Ndumo area), uMkhanyakude District, KwaZulu-Natal, South Africa (May 2014 to May 2015) (Adapted from Manyangadze et al., [11]) was semi-quantitative and was conducted by the same temperature, pH, salinity and conductivity were meas- two technicians using scoops made from a kitchen sieve ured using a portable water meter (Hanna Instruments, mounted on a broom stick [22, 23] and handpicking live Møllevænget, Sweden). Remote sensing data including visible snails for 30 min on each site [6]. Snails collected the climatic
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