Multilingual abstract

Please see Additional file 1 for the translation of the abstract into the five official working languages of the United Nations.

Background

Increasing evidence suggests that temperature rise may increase the spread of schistosomiasis [1, 2]. Nevertheless, the net effects of environmental changes involving temperature on the ecology of intermediate host (IH) snails remain a challenge to evaluate. Various laboratory experiments and statistical models continue to examine the potential effect of environmental changes on schistosomiasis [3,4,5,6,7]. These studies have provided important information on risk factors that influence Schistosoma infection even at micro-geographical scales [8]. In contrast, the prevalence of infection continues to be high, especially among poor and marginalised communities [9], thus indicating the need for increased health education, and the monitoring and surveillance of IH snail population dynamics.

Zambia is a country found in Southern Africa. It is landlocked and has 10 provinces. The burden of schistosomiasis in the country is still high despite efforts to reduce it [10, 11]. Schistosomiasis, commonly known as bilharzia, is caused either by Schistosoma haematobium or S. mansoni, and has been reported from various localities since the pre-independence era of the development of the healthcare system [12,13,14,15,16]. Several studies [17, 18] have reported cases of schistosomiasis in various parts of the country. Furthermore, earlier studies [15, 19] conducted in Siavonga, a town along the shores of Lake Kariba in the southern part of the country, observed an increase in the prevalence of S. mansoni and S. haematobium between 1993 and 1998. In the middle 1980s, certain parts of southern province had a prevalence rate of 57.9% [12].

Zambia has been experiencing changes in its environmental and socio-economic status [20]. These changes coupled with the predicted effect of climate change on IH snails [2,3,4,5,6, 21, 22] may alter the risk of Schistosoma infection [23, 24]. Currently, disease control strategies depend on mass drug administration (MDA) strategies [25, 26]. However, cases of re-infection and drug efficacy continue to be debated [27, 28] and this may be exacerbated by future climate change which may potentially proliferate Schistosoma production [1, 2, 7].

Taken together, these issues suggest the need to improve existing knowledge on schistosomiasis and identify knowledge gaps on the epidemiology of the disease. To achieve this, a systematic review and synthesis of literature was conducted to improve our understanding of the epidemiology and biogeography of schistosomiasis in Zambia. Existing evidence was summarised and research gaps for the control of schistosomiasis and IH snails were identified.

Methods

Search criteria

We carried out a systematic literature search on PubMed, Google Scholar and EBSCOhost for the period of 2000–2017 (see Fig. 1). The search considered studies that focused on human schistosomiasis and IH snails, Bulinus and Biomphalaria spp. and parasites, S. haematobium and S. mansoni in Zambia. The search was based on the combination of the following terms and Boolean operations: schistosomiasis AND Bulinus OR Biomphalaria snails AND Schistosoma haematobium OR Schistosoma mansoni in Zambia. More literature was also obtained using the snowballing technique: bibliographies or reference lists of previous reviews or similar studies that had been published in English were examined. Literature on studies that were conducted in other countries such as Zimbabwe but with data collected in Zambia were also obtained and used to strengthen the discussion and understanding of the bionomics of snails and the epidemiology of schistosomiasis. The search excluded articles that reported on schistosomes that infect ruminant animals. Articles that reported on S. mattheei, S. leiperi and S. margrebowiei were also excluded.

Fig. 1
figure 1

Selection criteria for articles used in the review

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The search criteria showed that most of the information on the bionomics of IH snails was from studies conducted in the 1950–1980 period [29]. This is an indication of a paucity of information on the epidemiology of the disease, which includes ecological changes that may have happened because of increased anthropological activities. Therefore, the search looked for articles that discussed disease risks in relation to IH snail bionomics, human-related, and environmental and climatic factors (see Fig. 1).

Results

Search results

The search procedure and results obtained are shown in Fig. 1. The search got 629 hits, with an additional nine articles added from snowballing to make a total of 638 articles. However, 625 articles were considered ineligible as they did not meet the inclusion criteria. The relevant articles were categorised based on their study focus. The categories were: malacology, socio-economics/demographics, clinical-based and modelling. The main findings from these articles are summarised in Table 1.

Table 1 Characteristics, objectives and outcomes of schistosomiasis studies focusing on Zambia that have been included in the review
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Two studies were malacology-based and explored the distribution of schistosomiasis in relation to snail availability. Six studies explored the prevalence of schistosomiasis by focusing on evaluating risk factors and linking them to socio-economic/demographic factors. These studies further collected parasitological information to determine disease prevalence. Three studies were clinical-based: one study collected biopsy specimen for analysis and another was a radiologically focused study. The third study focused on assessing the burden of hepatosplenic pathology and prevalence of S. mansoni infections. Other remaining studies evaluated infection risks based on the presence of Schistosoma antibodies in humans. Only two studies applied geospatial technology in understanding the epidemiology of the disease.

The selected studies suggest that schistosomiasis is prevalent and endemic in the country (see Fig. 2), and there is need to establish its prevalence in various parts of the country. According to Mubila and Rollinson [30], the prevalence of S. haematobium infection around Lake Kariba was 76%. Halwindi et al. [31] reported that the prevalence of the disease in Siavonga was 13.9%, with S. haematobium more prevalent than S. mansoni. Studies done in the western province reported more cases of S. mansoni than S. haematobium, with S. mansoni prevalent in 73% of the sampled individuals [32]. This is further reflected in the clinical-based study conducted by Payne et al. [33] which reported that 97% of the respondents tested positive for Schistosoma antibodies in their blood samples. The presence of schistosomiasis has also been reported in Zambezi, north-western province, where 37.2% of the children sampled were also in danger of peri-portal fibrosis due to S. mansoni infection [34]. Schistosomiasis has also been reported in Serenje (central province) [35] and in Lusaka [36,37,38] where prevalence rates of about 90.1% were observed in some communities [39] (see Table 1 and Fig. 2).

Fig. 2
figure 2

Map of Zambia showing the prevelance of schistosomiasis. Risk levels: low risk (≥1% and < 10%), medium risk (≥10% and < 50%) and high risk (≥50%). Source: Schistosomiasis Control Initiative [11]

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Various approaches have been used to study the epidemiology of schistosomiasis in Zambia. Monde et al. [40] explored the influence of various environmental factors on the abundance of IH snails, while Simoonga et al. [37] established a link between climatic variables and disease prevalence using a spatial-epidemiology approach. The study concluded that altitude, normalised difference vegetation index (NDVI), maximum temperature, age, sex of the child and IH snail abundance were the main factors contributing to disease prevalence. A statistical modelling approach using a hierarchical ordinal regression model was used by Simoonga and Kazembe [36] to further understand the influence of age, sex and altitude at which the child lived, NDVI, maximum temperature and snail abundance on infection risk. (see Table 1).

Although all studied have reported cases of schistosomiasis in both pre-urban and rural parts of Zambia, only Monde et al. [40], Chimbari et al. [41] and Mubila and Rollinson [30] have reported on the presence of IH snails.

Discussion

Biogeography of schistosomiasis in Zambia

Despite the implementation of disease control programmes [39] and the prospects of scaling them up [10], the prevalence of schistosomiasis may be higher than previously reported by Chitsulo et al. [13] and Zambia Bilharzia Control Programme [42]. Furthermore, schistosomiasis is prevalent and endemic across all 10 provinces [11] with S. haematobium endemic in 69 districts and S. mansoni in 49 districts [39]. The increase in the prevalence may be attributed to climate change [5], changes in livelihood strategies [40], religious and cultural practices which may influence human-water contact behaviours (e.g. baptism by immersion) and health-seeking behaviours [8, 38] and potentially perpetuate the maintenance of the parasite within the population [31].

The current study also indicates that the burden of morbidities associated with schistosomiasis in Zambia has not been fully explored. According to King and Dangerfield-Cha [43], schistosomiasis may present long-term health threats to the populations. Cases of peri-portal fibrosis among rural children in north-western province [34], peripheral fibrosis and main portal branch fibrosis in western province due to S. mansoni infection have been reported [44]. Additionally, Mutengo et al. [45] observed the presence of squamous cell carcinoma in cervical biopsies and genital malignancy among S. haematobium-infected individuals, which increases the risks of cervical cancer. Furthermore, infection with S. haematobium among women may lead to female genital schistosomiasis (FGS) [46], increase the risk of impaired reproductive organs [47] and HIV infection [48, 49]. The observed high prevalence of schistosomiasis in Zambia may indicate increased risk of both FGS and HIV infection especially among the women. This outcome suggests a need for guidelines and policy change in chemotherapy by also targeting the adult population group besides the school-age based population which for long has been the focus [50].

Scope of schistosomiasis studies conducted in Zambia since 2000

Many studies have evaluated the prevalence of schistosomiasis and its associated risk factors. Monde et al. [40] showed the relationship between various environmental factors and snail abundance. Other studies have also suggested that the transmission of schistosomiasis can also be influenced by IH snail-and parasite-related factors [51], temperature [7, 52, 53] and rainfall [54].

This review indicates that schistosomisis occurs within the socio-ecological system, therefore institutional factors are vital both in the spread and elimination of the diseases. Institutional factors such as policies, health infrastructure and developmental patterns may have long-and short-term effects on the economies of local communities and risk of infection [55]. These factors may influence the utilisation of health resources, and the development and deployment of effective control programmes. The current review suggests that there is a need to look at the epidemiology of schistosomiasis and contextualise aspects of institutional and ecological factors to suit the current disease control and elimination programmes.

Environmental factors and disease distribution

The effect of seasonal changes, ecology and the environment on schistosomiasis transmission in Zambia remains poorly understood. According to Utzinger et al. [56], ecological factors greatly influence the presence and abundance of IH snails and the development of the cercariae within them. Shiff et al. [57] and Manyangadze et al. [4] highlighted the seasonal population dynamics of IH snails. These studies indicated that the snail population reduces during the rain-season due to running water washing away the snails [58], while high water temperature and drying up of temporal water ponds induces mortality during the dry, hot seasons [29, 58], which also decreases the size of the snail population. Understanding these dynamics may aid efficient application of molluscicides and other snail control measures [57, 59].

In the study conducted by Simoonga et al. [37], the results showed that NDVI values between 128 and 160, and maximum temperatures of 20 °C to 21 °C increased the infection risk and enhanced the development of the snail-parasite system. This was corroborated by the findings of Manyangadze et al. [4] and Mukaratirwa et al. [60]. Except for studies conducted by Simoonga et al. [37] and Monde et al. [40], there is limited data on snail ecology, and environmental and climatic factors related to schistosomiasis transmission in Zambia. To effectively control schistosomiasis, MDA programmes should be accompanied by knowledge on the distribution and behaviour of IH snails [24, 61, 62]. This study therefore suggests the need of adopting recommendations by the Special Programme for Research and Training in Tropical Diseases to revive vector studies including snails [63, 64] within the country’s schistosomiasis programmes.

Using ecological models

The use of geographic information system (GIS) has been found to be essential in evaluating the suitability of specific areas for the development of the snail-parasite system, and monitoring of snail control programmes [24]. This is essential at the local level in Zambia where up-to-date parasitological data may not be readily available or difficult to access. Furthermore, the incorporation of GIS in predictive models has enhanced development of snail habitat suitability and distribution maps. These maps can be combined with suitable temperature regimes to define possible areas for the development of the snail-trematode system [24]. Such initiatives may increase the chances of successful implementation of health interventions in the context of limited resources.

Modelling approaches such as those explored by Simoonga et al. [37] and Simoonga and Kazembe [36] used robust statistical methods to explore possible uncertainties that may be associated with schistosomiasis intensity in Zambia. This review encourages the use of such models that account for the distribution of IH snails based on habitat suitability and intra-molluscan parasite development. Furthermore, modelling approaches used by Zhou et al. [2] and McCreesh et al. [5] to predict future changes in the geographical spread of IH snails are encouraged for effectively planning snail and disease control measures.

Policy implications

Schistosomiasis has been listed by WHO as a NTD, and there is need to eliminate it. This review has shown that the disease is endemic in Zambia and the need for treatment remains high. The new National Health Strategic Plan (2017–2021) acknowledges the impact of schistosomiasis and other NTDs, thus necessitating the need for national implementation of MDA.

In line with the recommendations by WHO, this review suggests the need to precisely map the distribution of the disease and IH snail distribution to support an effective MDA programme. The emphasis on snail populations is a recognition that snail populations may indicate potential transmission areas. Interventions targeted at snails in certain localities are possible. For instance, effective management of water for snail control was done in Zimbabwe (Mushandike Irrigation Scheme) [65]. The observed high prevalence of schistosomiasis among rural communities may indicate insufficient sanitary facilities and the use of contaminated water for domestic and recreational activities [31, 40, 25, 44].

Insights for public health professionals and possible directions for future control strategies

  1. 1.

    There is a need to tailor studies on understanding the probable impact of climate change on schistosomiasis risks. Human-driven anthropogenic activities and environmental change may alter the disease patterns and geographical range of IH snails [1, 2, 22]. Our review recommends the integration of socio-demographics, as well as environmental and IH snail-related factors to provide a better understanding of the possible impact of climate change on disease risks.

  2. 2.

    There is a need to develop predictive models that can be used to delineate present and potential future distribution and snail suitability areas to inform control measures. Due to a paucity of parasitological data, which makes determination of the actual disease prevalence difficult, predictive models that make use of both field-based and laboratory studies, as well as snail habitat suitability maps may be useful for indicating potential areas for disease risks. This will improve the design, implementation and monitoring of disease control measures.

  3. 3.

    Using the prevalence distribution map that was developed by the Schistosomiasis Control Initiative, there is a need to strengthen community engagement strategies through health education. Local-level institutions may also be strengthened to reduce the perpetuation of the parasite within the adult population [31, 50].

Conclusions

It is evident that schistosomiasis is prevalent in Zambia, and there is a need for researchers and disease control managers in the country, through inter-sectoral collaboration, to devise new control strategies and periodic disease surveillance programmes. This will increase the success of MDA programmes, which will be informed by disease distribution patterns. Furthermore, this review suggests the need to develop a specific action plan against schistosomiasis and devise applicable control measures for both children and adults to reduce the perpetuation of the parasite in the communities. Schistosomiasis occurs in the socio-ecological system, and therefore understating the epidemiology of the disease requires going beyond social determinants and including climatic variability and epidemiological niche modelling.