Zoonotic Schistosomiasis in Nigeria: The Concealed Threat to Humans Posed by Genetic Hybrid Parasites of Livestock Cattle Origin

Abstract

Schistosomiasis, also known as bilharzia, is a water-borne parasitic disease caused by blood flukes (trematode worms) of the genus Schistosoma. The disease is mainly found in tropical and subtropical regions, affecting more than 200 million people worldwide, but predominantly, about 90%, in sub-Saharan Africa. Nigeria shoulders the largest share of schistosomiasis cases on the African continent. While efforts to combat this disease have traditionally focused on human infections, there has been limited attention given to infections in livestock that might have the potential to spread to humans. Recent empirical findings indicate that, apart from Schistosoma species primarily associated with humans, there are schistosomes in livestock that can infect humans as well. This raises the possibility of genetic material mixing between cattle and human schistosomes, known as hybridization. This phenomenon poses a risk of zoonotic diseases transmission. This chapter delves into ongoing research concerning schistosome hybridization in Nigeria and elucidates its adverse effects on elimination endeavors. Furthermore, it explores the factors that encourage interactions between human and livestock schistosomes and outlines strategies for addressing these concerns.

1. Introduction

Schistosomiasis, historically referred to as bilharzia, is a significant neglected tropical disease (NTD) in sub-Saharan Africa [1, 2]. This parasitic disease is the result of infection by water-borne trematode worms, commonly known as blood flukes, belonging to the genus Schistosoma, which require specific aqueous snail intermediate hosts for their developmental cycle [3]. Currently, over 206 million people are affected in 78 countries across tropical and subtropical regions of Africa, the Middle East, some parts of Asia and Latin America [3], with approximately 24,000 deaths and 2.5 million disability-adjusted life years recorded annually [4]. Six schistosome species are known to exclusively infect humans, with four of them prevalent in Africa; Schistosoma guineensis, S. haematobium, S. intercalatum, and S. mansoni [3, 5]. Three other species, namely Schistosoma bovis, S. curassoni and S. mattheei, commonly infect bovids, including livestock cattle [5, 6]. The geographical distribution of these species collectively spans tropical and subtropical regions of Africa – including Nigeria that is discussed here [3].

Schistosomiasis primarily affects rural and marginalized urban populations that have frequent contact with surface water bodies, which may be infested with snail intermediate hosts. Lack of access to safe water, sanitation, and hygiene further exacerbates the risk of infection in these communities. Intestinal schistosomiasis is associated with most human schistosome species, while urogenital schistosomiasis is predominantly caused by S. haematobium [7]. Sub-Saharan Africa is home to approximately 90% of individuals affected by schistosomiasis who require treatment [3]. Nigeria, which has the largest population in the region of over 223 million, shas the highest number of schistosomiasis cases [1, 2].

The World Health Organization (WHO) has initiated a widespread distribution among at-risk school-age children of praziquantel, the primary drug deployed to treat schistosomiasis, as a way to reduce the extent of disease-associated morbidity [8]. This approach, known as preventive chemotherapy, aims to treat at least 75% of a community’s school-age children annually, in addition to implementing health education campaigns and snail reduction strategies [4]. However, the control of schistosomes that can be transmitted from livestock to humans, known as zoonotic schistosomiasis, has received little attention over the years [9]. This is particularly relevant in areas where the coexistence of humans, livestock, and suitable snail intermediate hosts occurs. Recent reports have highlighted the genetic hybridization of the closely related species S. haematobium and S. bovis that infects cattle [5, 10, 11], in several West African countries including Niger, Senegal, Mali, Benin, and Cameroon [11, 12, 13, 14, 15]. The migration of infected snails and the influx of livestock from neighboring countries into Nigeria raise concerns about the establishment of hybrid human urogenital and bovine intestinal schistosomes in Nigerian waters.

Schistosomiasis is a significant NTD in sub-Saharan Africa, particularly in Nigeria, which provides the focus of this chapter. The WHO-led preventive chemotherapy program has made progress in controlling the disease, but the control of zoonotic schistosomiasis remains a major challenge. The genetic hybridization of Schistosoma species, particularly S. haematobium x S. bovis, and the potential transmission from livestock to humans highlight the need for improved control programs and research to combat this neglected source of schistosomiasis more effectively.

2. Schistosoma haematobium life cycle

Schistosoma haematobium has two distinct life cycle phases, asexual and sexual. These involve infecting two different hosts, a snail intermediate host and a vertebrate definitive host, respectively. The cycle typically commences when eggs, discharged in the urine of an infected vertebrate host, encounter freshwater environments containing snails belonging to the Bulinus genus. Upon contact with water, the eggs hatch, liberating free-swimming miracidia, which then proceed to penetrate the snail host. Once established, these miracidia undergo asexual development through multiple stages, eventually becoming cercariae that leave the snail in search of the definitive host. Despite their short lifespan, a single miracidium in a suitable snail host can produce approximately 200 cercariae per day [16, 17].

The cercariae penetrate the skin of suitable definitive hosts that come into contact with the contaminated water, transforming into schistosomula. This penetration commonly takes place in surface water bodies that serve as gathering points for people and livestock, often used for domestic and recreational activities [18]. After penetrating the skin, the schistosomula migrate through the epidermis and dermis layers, eventually entering the bloodstream and traveling to the lungs [17, 19, 20, 21]. After leaving the lungs, the parasites reach the left side of the heart via the pulmonary veins and then enter the abdominal aorta. They can then pass through various arteries, such as the coeliac trunk, inferior and superior mesenteric arteries, or iliac arteries, to reach the portal veins of the liver [21]. In the liver, the schistosomula lose their migratory ability, grow, and develop into adult male and female pairs [21].

The adult worms, occurring in pairs, navigate against the natural flow of blood within the venous circulation. They eventually settle in the vesical venous plexus, a network of veins around the bladder. In this location, they produce eggs, which can migrate to various parts of the urinary tract, including the bladder and ureter [17, 21]. These eggs have the capability to penetrate the walls of blood vessels, the bladder, or genital organs [21]; those that make their way to the bladder are expelled from the body through urine into freshwater environments. In these aquatic settings, the hatched miracidia perpetuate the transmission cycle [17]. It is worth noting that other species of Schistosoma follow a comparable life cycle but may exhibit variations in their preferred sites and the morphology of their eggs [22]. These minor microscopical differences help diagnostic identification.

3. Zoonotic schistosomiasis

The classification of zoonoses or zoonotic diseases encompasses various infectious diseases and their causative agents that can be transmitted and established between human and animal hosts [23]. Therefore, zoonotic schistosomiasis refers to the presence of a Schistosoma species, which typically affects a specific human or animal host, in another host that is not specific to the schistosome group [12, 24]. These Schistosoma species are naturally shared between humans and various animal hosts due to the extensive interactions that occur at transmission sites [25, 26].

Hybridization can take place in regions where different schistosome species are either endemic or share substantial geographical overlap among potential hosts [27, 28]. These interactions between schistosomes can occur in two ways: bidirectional, whereby both male and female schistosomes from different pairs come together to produce viable hybrid offspring [24]; or unidirectional, in which pairing happens between schistosomes of either male or female sex [29, 30]. The establishment of hybridization has been observed in various studies, indicating the presence of hybrid schistosomes in both human and animal hosts [12]. These hybrids are not limited to first-generation offspring, which suggests the existence of stable hybrid zones. The occurrence of hybridization has implications for disease prevalence, pathology, and treatment, and may lead to the emergence of new pathogens, requiring additional control strategies [12, 24]. The understanding of hybridization and its impact on schistosomiasis is therefore crucial for effective control and prevention efforts.

4. Nigeria’s schistosomiasis control program

In 1995, the Nigerian Federal Government created the National Control Schistosomiasis Programme. Through epidemiological mapping, this revealed that at the time around 20 million people were infected with the disease. Pilot control projects were initiated in some selected states (Borno, Ebonyi, Katsina, Kwara, and Ondo), each having distinct ecological conditions that render them highly susceptible to schistosomiasis. Prevention and control activities have since evolved, being currently integrated into an expanded program that aims to eradicate other neglected tropical diseases [31]. This has driven mass drug administration (MDA) of praziquantel with the support of organizations such as the WHO, UNICEF, and various non-governmental development organizations. MDA is carried out at the level of implementation units (IUs), which can be a district, province, or local government area [8]. Disease prevalence and population data at the community level are aggregated at the IU level to determine praziquantel treatment thresholds [8, 32].

Praziquantel MDA is administered every six months to all school-age children in districts where the prevalence exceeds 50%, annually for districts with a prevalence ranging from 10% to 49.9%, and every two years for districts with a prevalence between 1% and 10% [8]. However, recently published WHO guidelines have revised these recommendations, specifying annual MDA for all school-age children with a prevalence above 50%, biennial MDA for half the children with a prevalence between 10 and 49.9%, and two treatments during primary schooling for all children with a prevalence between 1 and 10% [33]. In 2019, approximately 250 million praziquantel doses were used to treat 95.3 million children and adults, achieving an epidemiological coverage of 67% [4]. This falls short of the 75% target set for 2020, emphasizing the need to accelerate progress in control and prevention. The 2020–2030 global NTD elimination roadmap sets more specific targets for schistosomiasis, including reducing the proportion of moderate and heavy intensity infections to less than 1% in 78 countries, reducing the number of tablets required during MDA by 50%, and increasing domestic financial support for MDA [3, 4]. Achieving these targets largely depends on increased community participation, geographical reach, and high program coverage during MDA [34, 35, 36, 37].

5. Impact of hybridization on schistosomiasis control efforts

The presence of hybrid schistosomes is a significant concern for the schistosomiasis control program in Nigeria, as it can lead to a wider host range, increased transmission potential, altered pathology, and potential drug resistance [38]. Interactions between different Schistosoma species can enhance reproductive capacity, resulting in a higher number of parasite offspring, faster maturation, and a broader range of intermediate hosts [39, 40]. One major concern is that the emergence of hybrid schistosomes may reduce the effectiveness of praziquantel treatment [41]. This phenomenon has been documented in both real-world field settings and controlled laboratory environments, particularly in the case of S. mansoni. It is closely linked to the concealed or hidden role that hybridization plays in this context [42, 43, 44]. The success of praziquantel as a treatment is therefore threatened by the presence of Schistosoma hybrids [5]. Additionally, the genetic diversity among progeny of zoonotic schistosomes provides them with better phenotypic characteristics [45], allowing for improved evasion of host recognition and resistance to the host’s adaptive immune system. This can result in increased infectivity and the development of unusual pathologies [46]. The infection of multiple animal reservoir hosts by zoonotic hybrid schistosomes makes the elimination of the disease more challenging [14, 15]. The ubiquitous presence of rodents, which serve as reservoir hosts for many schistosome species, contributes to the difficulty in controlling and preventing Schistosoma hybrid infections in endemic areas due to the potential for co-infection [47].

6. Factors promoting hybridization of schistosome species

6.1 Shared freshwater bodies and occurrence of weather events

Schistosomiasis is a disease that primarily occurs in specific areas with slow-moving freshwater bodies that support the proliferation of intermediate host snails. This is particularly evident in locations where dams and similar water development structures are present [48, 49]. However, changes in environmental and climatic conditions have the potential to expand the geographical range of the disease [50]. Unprecedented transmission of schistosomiasis has been observed at higher altitudes in Uganda, where clinical infection would not typically be expected [51]. Studies from eastern Africa and China have also predicted that rising ambient temperatures could impact schistosomiasis transmission [52, 53].

It is likely that fluctuations in schistosomiasis transmission will be observed in areas bordering currently endemic regions [54]. Additionally, geographically disconnected but endemic communities may share ecological links through common rivers, streams, or other freshwater bodies. This creates a window of opportunity for schistosomes and their intermediate hosts to establish themselves in novel locations, particularly during weather-related events such as flooding. Studies conducted in China have revealed that significant flood disasters can lead to the dispersal and establishment of new populations of intermediate host snails in regions where schistosomiasis was not previously present or had been previously eliminated [52]. Similar outbreaks have been observed in Nigeria after flooding [55]. The presence of large rivers that transcend international boundaries further increases the possibility of hybrid schistosomes being introduced to new areas. The Niger River, for example, passes through multiple countries, including Nigeria, and has been associated with the hybridization of S. haematobium and S. bovis species. The establishment of hybrid schistosomes and zoonotic infections in endemic areas affected by flooding requires close surveillance.

Despite ongoing preventive chemotherapy programs, schistosomiasis transmission continues in some endemic areas in Nigeria [48, 56]. The Niger River, being the longest river in West Africa, poses a significant challenge for control efforts due to its extensive reach and the high population density in its delta region. The emergence of hybrid schistosomes in areas sharing the Niger River and its tributaries with neighboring countries increases the risk of hybrid schistosomes being introduced to Nigeria during flooding events [57]. The surveillance of schistosome hybrid species and zoonotic infections in flood-affected endemic areas is crucial for effective control and prevention.

6.2 Water development projects and flooding

In 2017, the Federal Ministry of Agriculture and Rural Development in Nigeria estimated that the country’s livestock production encompassed a substantial population, which included approximately 18.4 million cattle, 43.4 million sheep, 76 million goats, and a staggering 180 million poultry [58]. Small-scale livestock holders and nomadic herders play a significant role in this production [59]. It is estimated that 13 million households, accounting for 42% of the Nigerian population, own livestock. Similar to other regions in the developing world, cattle and other livestock in rural Nigeria often live in close proximity to humans and freely roam within the local community [60]. This close ecological interaction between humans and animals, particularly through shared resources like water, creates an environment conducive to the zoonotic transmission of pathogens. Schistosomiasis transmission is closely linked to the presence of freshwater bodies that support vector snails, and zoonotic transmission occurs in areas where humans and animals have close ecological interactions.

Hybrid schistosomes have been detected in children residing in villages located around the Senegal River Basin in Senegal. This occurrence is closely linked to water development projects that have expanded shared water interactions between humans and livestock in the region [12]. These hybrids result from the hybridization of human and bovine schistosomes (S. haematobium and S. bovis), providing evidence of zoonotic Schistosoma infection between humans and cattle. Similar outbreaks of schistosomiasis have been reported in Nigeria following major water development projects and flooding events [61, 62, 63, 64]. However, the potential changes in zoonotic transmission dynamics resulting from altered human-animal interactions in affected areas have not been thoroughly investigated. Despite the demonstrated ability of locally endemic species like S. mansoni to infect a broad range of hosts, including rodents and primates, there has been limited interest in the zoonotic transmission of schistosomes in Nigeria [25, 65]. This highlights the need for further research and surveillance to understand and address the zoonotic transmission of schistosomiasis in the country.

6.3 In-country and cross-border migration of livestock

Understanding the transmission of zoonotic schistosomes is of utmost importance in Nigeria, where livestock production is dominated by nomadic pastoral practices. This farming method accounts for approximately 82% of the country’s cattle [60], primarily owned by the Fulani population, who are known for their nomadic lifestyle [66]. The Fulani people are renowned as the world’s largest nomadic ethnic group and hold a prominent position in Nigeria as the nation’s leading pastoralists [67, 68].

In addition to various other nomadic groups, the Fulani make up approximately 12% of the population in sub-Saharan Africa [69]. These nomadic communities depend entirely on livestock for their livelihoods and sustenance. They engage in a migratory lifestyle, crossing national boundaries as they seek pasture and freshwater resources essential for the wellbeing of their herds [70, 71]. This seasonal movement, known as transhumance herding, is believed to contribute to the spread of the Rhipicephalus (Boophilus) microplus tick across Africa. The emergence of this tick in new areas, such as Nigeria, is attributed to pasture rotation practices aimed at managing tick populations [72]. Rhipicephalus microplus serves as a vector for the protozoan pathogen that causes bovine babesiosis, a significant disease in cattle. Hence, the dependence of pastoralist communities on water resources during their migrations elevates the risk of introducing both Schistosoma and Babesia to new regions of Nigeria where these parasites were not previously considered threats to public or veterinary health.

The movement of hosts also has the potential to disrupt the natural distribution of schistosome species and raise the likelihood of interbreeding between different species [40]. In addition to internal migration, the entry of livestock from neighboring countries within the Economic Community of West African States, for purposes such as trade and open grazing, further facilitates the potential introduction and establishment of hybrid schistosomes within Nigeria’s river systems. This is especially pertinent to regions where hybridization has been documented. The contamination of Nigeria’s water bodies by migrating livestock from both domestic sources and trans-border routes poses a major challenge to schistosomiasis control initiatives.

6.4 Inadequate clean water, sanitation, and hygiene facilities

Schistosomiasis is categorized as an NTD because it disproportionately affects socioeconomically disadvantaged populations worldwide [73]. In Nigeria, over 83 million people live in extreme poverty, lacking access to clean water, sanitation, and hygiene (WASH) facilities, as well as other basic social amenities [74]. These communities heavily rely on agriculture, with 70% engaging in livestock rearing for their livelihoods [75]. According to data from the World Bank, it is estimated that about 39% of rural domiciles in Nigeria do not have access to safe water sources. Additionally, only 50% of these households have access to improved sanitation facilities, and approximately one-third of them still engage in open defecation practices [76]. In most cases, the primary water sources for these communities are freshwater bodies located nearby, which are frequently contaminated due to poor sanitation conditions and practices [48]. The socioeconomic circumstances make it challenging to develop separate water sources for humans and animals, leading to continued co-interaction at open water bodies, posing a significant public health challenge. This situation significantly elevates the risk of zoonotic transmission of schistosomiasis between different hosts.

Recognizing the critical state of WASH facilities in Nigeria, the Federal Government has taken steps to address the issue and promote equitable access to improved WASH facilities [77, 78]. One notable initiative is the National Urban Water Sector Reform Program, which has constructed more than 2300 water points across the country since 2015, with a primary focus on urban areas [76]. Unfortunately, this urban-centric approach has left rural areas with profoundly inadequate coverage, thereby exacerbating the challenge of providing WASH facilities to rural communities through the existing Rural Water Supply and Sanitation Programme [79]. In response to this situation, in 2018 the Federal Government declared a state of emergency in the country’s drinking water, sanitation, and hygiene sector. One critical issue identified was that many water supply pumps installed in rural areas fail shortly after installation and remain unrepaired, leaving the population without access to clean water [80]. This underscores the urgent need for more sustainable approaches to providing safe drinking water to rural communities.

Research has demonstrated that the availability of WASH facilities is associated with a reduction in NTDs such as soil-transmitted helminth infections and schistosomiasis [81, 82]. Providing WASH facilities in schistosomiasis-endemic communities not only prevents the sharing of water between humans and animals, thereby reducing the risk of zoonotic infections, but also brings broader health benefits. It is imperative to assess the impact of expanding access to WASH facilities in schistosomiasis-endemic areas of Nigeria, both in terms of reducing the transmission of Schistosoma species to humans and the potential for zoonotic transmission between humans and animals.

7. Future research priorities

Limited information is available on the epidemiology of hybrid schistosomes in Nigeria [83]. Recent reports have provided some morphological characterization of hybrid Schistosoma eggs in endemic areas of southwestern Nigeria. However, further research is needed to obtain detailed and confirmatory evidence regarding their genetic diversity [84]. This information is crucial for informing programming and policy decisions, particularly regarding the efficacy of praziquantel. Conducting such investigations would require access to state-of-the-art facilities and the development of research capacity, which is currently lacking or inadequate [85].

8. Conclusions

Investing in adequate water, sanitation, and hygiene (WASH) facilities and implementing effective strategies to modify habitats and prevent flooding are crucial for controlling schistosomiasis in Nigeria. However, in addition to providing these resources, it is recommended to implement innovative health education programs that promote optimal usage and sustainable maintenance among the targeted nomadic communities. These outreach programs should involve consultation with community leaders to incorporate local livestock rearing strategies that prevent contamination of communal water bodies with human and livestock waste. By taking these measures, the risk of genetic hybridization by schistosome species of different origin can be significantly reduced. Furthermore, it is crucial to establish accurate surveillance systems, promptly detect outbreaks, identify Schistosoma species, and consistently promote preventive chemotherapy as integral activities of a nationwide schistosomiasis control program in Nigeria.

Conflict of interest

No conflicts of interest declared.

Author contributions

All authors contributed significantly to preparing and writing this chapter.

Funding statement

No specific funding was received for this work.