Schistosomiasis with a Focus on Africa
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Tropical Medicine and Infectious Disease Review Schistosomiasis with a Focus on Africa Oyime Poise Aula 1,2,* , Donald P. McManus 1 , Malcolm K. Jones 3 and Catherine A. Gordon 1,* 1 School of Public Health, Faculty of Medicine, University of Queensland, Brisbane 4006, Australia; [email protected] 2 Molecular Parasitology Laboratory, QIMR Berghofer Medical Research Institute, Brisbane 4006, Australia 3 School of Veterinary Sciences, University of Queensland, Gatton 4343, Australia; [email protected] * Correspondence: [email protected] (O.P.A.); [email protected] (C.A.G.) Abstract: Schistosomiasis is a common neglected tropical disease of impoverished people and livestock in many developing countries in tropical Africa, the Middle East, Asia, and Latin America. Substantial progress has been made in controlling schistosomiasis in some African countries, but the disease still prevails in most parts of sub-Saharan Africa with an estimated 800 million people at risk of infection. Current control strategies rely primarily on treatment with praziquantel, as no vaccine is available; however, treatment alone does not prevent reinfection. There has been emphasis on the use of integrated approaches in the control and elimination of the disease in recent years with the development of health infrastructure and health education. However, there is a need to evaluate the present status of African schistosomiasis, primarily caused by Schistosoma mansoni and S. haematobium, and the factors affecting the disease as the basis for developing more effective control and elimination strategies in the future. This review provides an historical perspective of schistosomiasis in Africa and discusses the current status of control efforts in those countries where the disease is endemic. Citation: Aula, O.P.; McManus, D.P.; Jones, M.K.; Gordon, C.A. Keywords: schistosomiasis; Schistosoma haematobium; Schistosoma mansoni; sub-Saharan Africa; Africa Schistosomiasis with a Focus on Africa. Trop. Med. Infect. Dis. 2021, 6, 109. https://doi.org/10.3390/ tropicalmed6030109 1. Introduction Schistosomiasis is a snail borne, fresh water-transmitted neglected tropical disease Academic Editors: Constantinos Tsioutis and (NTD) of poverty in many developing countries in tropical and sub-tropical Africa, the Spyridon Karageorgos Middle East, Asia, and Latin America [1–3] (Table1). The disease is generally endemic in low-income rural communities without access to potable water, proper sanitation, and Received: 13 May 2021 adequate healthcare facilities. Sub-Saharan Africa (SSA) constitutes about 13% of the Accepted: 4 June 2021 world’s population but accounts for up to 90% of cases with an estimated 280,000 deaths Published: 22 June 2021 due to schistosomiasis annually [2]. The two major species infecting humans in sub- Saharan Africa are Schistosoma haematobium, which causes urogenital schistosomiasis and Publisher’s Note: MDPI stays neutral S. mansoni, the cause of intestinal schistosomiasis. S. intercalatum and S. guineensis also with regard to jurisdictional claims in cause intestinal schistosomiasis but are less prevalent (Table1)[ 4]. Similarly, the main published maps and institutional affil- schistosome species infecting animals are S. mattheei, S. bovis and S. currassoni (Table1). In iations. recent years, there have been cases of locally acquired urinary schistosomiasis cases caused by S. haematobium reported in Corsica, France where it had previously not been endemic, likely imported by individuals infected in West Africa [5,6]. There is also increasing evidence of hybridization events between human and animal schistosome species, leading Copyright: © 2021 by the authors. to new zoonotic infections [7–9]. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Trop. Med. Infect. Dis. 2021, 6, 109. https://doi.org/10.3390/tropicalmed6030109 https://www.mdpi.com/journal/tropicalmed Trop. Med. Infect. Dis. 2021, 6, 109 2 of 40 Table 1. African schistosome species and their geographical distribution. Species Intermediate Geographical Host Definitive Hosts Site of Infection Distribution References Sub-Saharan Africa, Madagascar, the S. mansoni Biomphalari spp. Intestinal Humans, rodents mesenteric veins Middle East, [1,10] the Caribbean, Intestinal South America schistosomiasis Humans, S. intercalatum non-human Bulinus spp. Intestinal Central Africa, West and S. guineensis primates mesenteric veins Africa, Madagascar [1,10,11] (excluding apes) Humans, non-human Sub-Saharan Africa, Urogenital S. haematobium Bulinus schistosomiasis spp. primates Urogenital veins the Middle East, [1,10] Corsica (France) (excluding apes) S. mattheei Bulinus spp. Cattle, sheep, Intestinal Southeastern and goats mesenteric veins Central Africa [12–15] S. curassoni Bulinus spp. Cattle, sheep, Intestinal West Africa [12–15] Animal goats mesenteric veins intestinal schistosomiasis North, East, West Cattle, goats, and Central Africa, S. bovis Bulinus spp. Intestinal sheep, horses, mesenteric veins the Middle East and [12–15] camels, pigs Mediterranean (Europe) region Schistosomiasis control programs in Africa focus predominantly on community-based preventive chemotherapy (PC), focusing on mass drug administration (MDA) with prazi- quantel (PZQ), a broad spectrum anthelminthic, to reduce morbidity. Every year PZQ is do- nated to endemic countries in Africa to treat millions of school-aged children (SAC) [16,17]. Treatment compliance is challenging, especially among individuals in low socioeconomic areas due to fear of adverse effects, apparent absence of disease symptoms, and even when symptoms occur, they are often met with stigmatisation [18,19] or seen as a normal sign of puberty [20,21] not requiring treatment. There have been increased efforts aimed at eliminating schistosomiasis in the past decade with the World Health Organization (WHO) setting 2030 as the goal for transmission interruption in endemic African countries [22]. Government agencies from many countries have prioritised the control of NTDs by ex- ploiting breakpoints in their lifecycles, such as the implementation of snail control and through improvements in sanitation and access to safe, clean water [23,24]. However, in sub-Saharan Africa, PC is still the major intervention practiced. As PZQ is ineffective against migrating schistosomula, if these larvae are present in an individual, treatment may not prevent their maturation to adults and resultant patency. Rapid re-infection following treatment with PZQ is also common [25–27]. SAC are the main targets for control as they are considered to be at the highest risk of infection, being more likely to participate in daily activities including fishing, rice farming and swimming, that put them at greater risk of infection compared with other age groups. Protective immune responses against schistosomes develop slowly, with children from schistosomiasis-endemic areas being generally susceptible to reinfection after treatment for schistosome infection, whereas adults are usually protected [10]. This observation can explain the characteristic age-prevalence and age-intensity curves observed in schistosomiasis-endemic areas in Africa [11,28,29]. 2. Pathogenesis 2.1. Life Cycle of Schistosoma sp. Schistosomes have a complex life cycle involving both intermediate gastropod hosts and a definitive mammalian host (Figure1). Unlike other trematode species, Schistosoma spp. are dioecious (separate male and female worms) which undergo sexual reproduction in the mammalian definitive host. Schistosome eggs are produced and excreted into the environement via the faeces (S. mansoni) or urine (S. haematobium). Miracidia are released Trop. Med. Infect. Dis. 2021, 6, x FOR PEER REVIEW 3 of 39 Schistosomes have a complex life cycle involving both intermediate gastropod hosts and a definitive mammalian host (Figure 1). Unlike other trematode species, Schistosoma spp. are dioecious (separate male and female worms) which undergo sexual reproduction in the mammalian definitive host. Schistosome eggs are produced and excreted into the Trop. Med. Infect. Dis. 2021, 6, 109 environement via the faeces (S. mansoni) or urine (S. haematobium). Miracidia3 of 40 are released when the eggs come in contact with water and infect the snail host. There, miracidia de‐ velops into mother sporocysts and undergo asexual reproduction to produce daughter sporocysts which produce cecariae. Infected snails shed cercariae into the water and upon when the eggslocating come a insuitable contact definitive with water host, and penetrate infect the the snail skin, host. transform There, into miracidia schistosomula and develops intomigrate mother through sporocysts the circulatory and undergo system asexual to reproductionthe lungs, heart to produceand liver daughter where they mature sporocysts whichinto adult produce worms cecariae. (Figure Infected 1). The snails adult shed worms cercariae then exit into the the liver water and and pair upon up to mate in locating a suitablethe mesenteric definitive vessels host, penetrateof the bowel the ( skin,S. mansoni, transform S. intercalatum into schistosomula) or bladder and (S. haemato‐ migrate throughbium). the circulatory system to the lungs, heart and liver where they mature into adult worms (Figure1). The adult worms then exit the liver and pair up to mate in the mesenteric