| Abstract|| |
Cryptosporidium spp. are associated with diarrheal disease which leads to nutritional deficiencies and significant morbidity and mortality in children and patients with immune defects. The continuous emergence and molecular diversity of Cryptosporidium spp. still remains a threat to human health in respect of diarrhea and malnutrition in children <5 years. The impact of the cryptosporidiosis is exacerbated by the spread of human immunodeficiency virus/AIDS, and water shortage in most part of Southern Africa and the burden of the disease is underestimated within the region. Both anthroponotic and zoonotic transmission are identified as a common transmission route. Molecular characterization of Cryptosporidium infection is still a challenge, and there is a paucity of information on the burden of the parasite in Southern Africa. Ongoing attempts to find appropriate drugs and vaccines to cure and prevent the spread of the disease have limitations; perhaps considering isolation of bioactive compounds from medicinal plants extracts for their effectiveness and potency may be an option in future to control and eliminate the disease. This review considered the prevalence and molecular diversity in respect of transmission routes and associated risk factors. Urgent assessment of public health significance of this parasite in Southern Africa and elsewhere is of utmost importance. It is apparent that there is a need for adequate surveillance in monitoring the pathogen and to control the spread of infection.
Keywords: Animal, Cryptosporidium, epidemiology, human, prevalence, Southern Africa, waterborne
|How to cite this article:|
Ojuromi OT, Ashafa AO. Cryptosporidiosis in Southern Africa: Review of prevalence and molecular epidemiology of a neglected disease. Ann Trop Med Public Health 2018;11:108-18
|How to cite this URL:|
Ojuromi OT, Ashafa AO. Cryptosporidiosis in Southern Africa: Review of prevalence and molecular epidemiology of a neglected disease. Ann Trop Med Public Health [serial online] 2018 [cited 2020 Aug 3];11:108-18. Available from: http://www.atmph.org/text.asp?2018/11/4/108/272555
| Introduction|| |
Burden of Human Immunodeficiency Virus, Diarrhea, and Malnutrition
The estimated African population is expected to be around 1.2 billion people in few years. The Southern African countries make up about 35% of the total population of Africa with the prevalence rate of human immunodeficiency virus (HIV) between 1.0% and 26.5% in 2011. Adult HIV prevalence exceeded 20% in Swaziland, Botswana, and Lesotho. In terms of HIV case number, South Africa has the largest population of people living with HIV (6.3 million) in Southern Africa [Figure 1].
|Figure 1: Distribution of population, human immunodeficiency virus, and access to portable water (source: World Bank, United Nations Statistics Division, UNAIDS, UNICEF)|
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Infectious diseases in developing countries cause enormous morbidity and mortality, and diarrheal disease in Sub-Saharan Africa accounts for 16% of deaths in African children <5 years, which is amplified by HIV epidemic. Although Southern African region may have up to 71% of all people living with HIV, it is still spreading in the region and remains disproportionately affected by the epidemic. The same countries are home to 31% of people newly infected with HIV and 34% of people dying from AIDS-related causes. Antiretroviral coverage increased from 24% to 54% in 2015, reaching a regional total of 10.3 million people. For example, South Africa had nearly 3.4 million people on treatment more than any other country in the world. Botswana, Kenya, Malawi, Mozambique, South Africa, Swaziland, United Republic of Tanzania, Zambia, and Zimbabwe all increased treatment coverage by more than 25 percentage point between 2010 and 2015. Part of sustainable development goals was ending all forms of malnutrition (stunting, wasting, and overweight) among children <5 years. Globally, in 2015, almost one in four children under 5 years of age (156 million children) were affected by stunting. and wasting was prevalent in the WHO South-East region. Studies have demonstrated that poverty, malnutrition, and Cryptosporidium infection remain intricately connected,, and there is a need to confirm such in Southern Africa. Studies have shown that stunted growth in the first 2 years has overbearing effects on growth and development.,,,,, However, where Cryptosporidium is found in high prevalence among children, the best strategy is to treat infected people to reduce the spread of infection. The recommended drugs of choice for the treatment of cryptosporidiosis in immune-deficient human patients are nitazoxanide and paromomycin. Halofuginone is approved in Europe for prophylactic treatment of calves. Nitazoxanide has a broad spectrum of activity against many other gastrointestinal pathogens; however, it is not effective against Cryptosporidium in immunocompromised persons. This review attempts to address the public health significance of Cryptosporidium infection and its attendance implication in health care.
| Human Cryptosporidiosis-Associated Diarrhea and Malnutrition in Southern African Countries|| |
Cryptosporidium spp. are enteric protozoa with over 27 species described, but Cryptosporidium hominis and Cryptosporidium parvum most commonly infect humans.,, There are over 40 genotypes with a high probability that many of these will eventually be given species status with increased biological and molecular characterization. It is estimated that nearly 1.7 billion cases of diarrheal disease occur yearly, the leading cause of malnutrition in children under 5 years old and 2.6 billion lack improved sanitation and this may likely double by 2025. However, diarrhea incidence and case-fatality ratios are much higher within low-income countries than in middle- and high-income countries. Fifteen countries in Africa account for 53% of the total episodes of diarrhea globally, 56% of severe episodes, and 74% of the total burden of diarrhea mortality in children <5 years.
Cryptosporidium is still an emerging pathogen and continuously identified as the cause of multiple diarrhea in developed and developing countries.,,,,,, The Global Enteric Multicenter (GEM) assessed the cause, burden, clinical syndrome, and adverse outcomes of moderate-to-severe diarrhea in children at several sites in Sub-Saharan Africa and South Asia and identified Cryptosporidium as one of the four major contributions to moderate-to-severe diarrheal diseases during the first 2 years of life at all the sites. Previous reports corroborate the GEM observation in Southern Africa and elsewhere.,,,,,, Some longitudinal and cross-sectional studies have consistently shown that <5 years are associated with high-risk infection.,, In addition, several authors have opined that unsafe water, sanitation, and hygiene conditions facilitate the transmission of enteric pathogens from infected individuals to a new susceptible host through direct contact and/or through the environment.,,,,,,,,,
| Epidemiology in Children|| |
Despite so much knowledge of the distribution of Cryptosporidium spp. in the developed countries, there is still a gap in understanding the route of transmission, prevalence, and molecular epidemiology of the disease in most part of Sub-Saharan Africa, especially Southern African countries. One of the most common intestinal opportunistic parasites is Cryptosporidium and is listed as an AIDS-defining illness by the US Center for Disease Control and Prevention., Globally, the prevalence rate of Cryptosporidium infection may account for 10%–20% of the cases of diarrhea in HIV-infected patients living in developed countries and up to 50% in impecunious countries.,,, Diarrhea has been recognized as a persistent, seasonally occurring disease in Chobe District, Botswana. Cryptosporidium infection frequently produces severe to chronic diarrhea with intestinal dysfunction leading to malnutrition even in healthy children., The parasite was implicated in an epidemiological review of enteropathogens with the prevalence rates of 2.2% in Gaborone, Botswana. Another study investigated mortality among nonbreastfed children during diarrhea outbreak and malnutrition; stool examination generated numerous pathogens of which 60% had Cryptosporidium (50% C. parvum and 41% C. hominis). According to the report, the effects of diarrhea were more pronounced in HIV-negative, not breastfed and malnourished children. These factors were considered important elements to their severe illness and death. Other studies reported various prevalence in children <5 years with more positive cases during diarrhea outbreak.,, This indicates that Cryptosporidium infection is a potential cause of diarrheal disease in children within these communities and confirms that public health education must include an emphasis on improved sanitation practices in a household with diarrhea and surveillance should be directed at under and above 5 years age group in areas of high HIV prevalence. Shortage of quality water was identified as the major cause of diarrhea outbreak in Botswana.
An extensive study from Madagascar confirmed the predominance of C. hominis in children with diarrhea and the disease (cryptosporidiosis) accounted for 5.6% of the diarrhea cases in these group of children. The subtypes identified are Ia, Id, Ie, and IIc associated with anthroponotic transmission. However, there is a high possibility of identifying more species with large-scale study involving animals and environmental samples. Diarrhea, acute respiratory infection, malaria, and fever are among the leading causes of childhood mortality and morbidity in Malawi and elsewhere in Africa.,, According to Morse et al., up to 10% of diarrhea in children aged <5 years was attributed to Cryptosporidium spp. infection with up to 21% reported in immunocompromised population. Evidence from a molecular diversity of Cryptosporidium infection was attributed to increased zoonotic exposure and malnutrition. This indicates the need to improve on water supply, sanitation, household hygiene, and animal control. Subsequently, molecular characterization identified C. hominis and C. parvum and sequence analysis established high intraspecific variations of C. hominis subtypes and anthroponotic transmission was associated with cryptosporidiosis.,
Few studies have identified Cryptosporidium in some provinces of South Africa,,,,,, as the causative agent of diarrheal disease in immunocompetent, HIV-positive children and adults. From such studies, Cryptosporidium was found more in children <5 years and sometimes coexist with Giardia infection., Furthermore, Leav et al. identified species and genotypes of Cryptosporidium isolates from HIV-infected children in Durban and 15 isolates of genotype I allele (Ia, Ib, Ic, and Id) and 5 displayed a novel genotype Ie of C. parvum. Some of the isolates manifested unusual chimeric genotype Ib, Ic, or Ic/II allele, raising concern about the possibility of sexual recombination within and between parasite genotypes. In Limpopo Province, Cryptosporidium was found among children, and hospital patients and C. hominis were predominantly common than C. parvum, but genotypic identification was unaccomplished to confirm zoonotic or anthroponotic transmission. The importance of Cryptosporidium and Giardia infection was confirmed in another survey. Such finding confirms that both organisms are highly associated with diarrhea in some parts of South Africa. Molecular analyses from four provinces identified C. hominis (76.0%) with subtypes families (Ia, Ib, Id, Ie, and If), C. parvum (20%) with three subtypes family (IIc, IIe, and IIb), and subtype IIc being the most common. In contrast, Cryptosporidium meleagridis of subtype family IIId was identified in other studies, a parasite originally described in turkeys and humans.,,, Thus Confirming C. hominis and anthroponotic C. parvum subtypes are common in South Africa. Collectively from these studies, anthroponotic and zoonotic transmissions are common in some of the provinces studied.
Considering the level of HIV infection in Swaziland, information on the burden of cryptosporidiosis is still inadequate. The first report of Cryptosporidium infection in Swaziland gave an infection rate of 4.2% from the diarrheic stool of pediatric outpatients. In our view, there is lack of information about cryptosporidiosis infection in this country considering the level of HIV/AIDS. In contrast, Moyo et al. reported the prevalence of 18.9% Cryptosporidium infection in children hospitalized for diarrhea in Tanzania which was higher than that of Cegielski et al. The high rate of infection was attributed to the presence of C. parvum and other enteropathogenic organisms. Another study examined 108 women and infants in rural/semi-rural Tanzania and noted the high level of maternal Cryptosporidium infection (63%) among the participants. It was noted that Cryptosporidium in infants increased dramatically between 3 and 6 months of age, a period that corresponds to changes in breastfeeding practices. Reiterating the fact that infants residing in rural and semi-rural areas are more susceptible to Cryptosporidium infection in early infancy with approximately 1/3 of infants showing evidence of infection by 6 months of age., Invariably, concerted efforts must be geared toward understanding the public health significance of the pathogenic parasite to humans and animals in these countries.
Annual rainfall reductions in the Southern Africa region and increased human consumption have contributed immensely to water shortage. Seasonal peaks in cryptosporidiosis have been reported in several Sub-Saharan countries. In a report from Durban, South Africa,Cryptosporidium infection was associated with seasonal variation, especially during the dry and wet season. High prevalence of infection was associated low-income settings and rainy season. The nonavailability of good drinking water during dry season may compound the spread of infection, thereby necessitating people within a community to consume water from protected and unprotected water sources that may have been contaminated with this parasite and other enteric pathogens.
Cryptosporidium infection is greatly compounded by HIV infection and malnutrition in Sub-Saharan Africa. Among HIV-positive children in Zambia with persistent diarrhea and malnutrition, C. parvum was the dominant species when compared with other intestinal infectious agents. Based on previous reports, the prevalence rate of infection ranged from 18% to 32%.,,,,, The astonishingly high rate in children with persistent diarrhea, malnutrition syndrome, particularly the impact of cryptosporidiosis, and salmonellosis contributes to pathophysiology among the studied population. Within the same region, C. parvum was found in 18.0% of children who presented with diarrhea; most of the children had acute illnesses., Another study determined the prevalence, incidence, and seasonal variation of Cryptosporidium and Giardia intestinalis from preschool children in Kafue, Zambia,Cryptosporidium (30.75%) and Giardia (29.0%) infections were documented, and diarrhea was significantly associated with cryptosporidiosis than giardiasis. The prevalence of more than 80% of Zambian children being parasitized with Cryptosporidium is remarkable and supported a seasonal increase in cryptosporidiosis during the rainy season.,
| Epidemiology in Human Immunodeficiency Virus Patients|| |
Enteric opportunistic parasites are associated with HIV/AIDS, chronic diarrhea, education, occupation and residence in a slum, exposure to pets and animals, antiretroviral therapy, use of public toilets, water and practicing unsafe homosexual activity.,,,,,, Few studies in Congo,, determined the prevalence and species spectrum of intestinal parasites (IP) in hospitalized AIDs patients. Diarrhea was a common syndrome in 49.7% patients hospitalized, 26.9% harbor an IP, and 15.4% were infected with at least one opportunistic IP and 9.7% with Cryptosporidium infection. Unsurprisingly, coinfection of Cryptosporidium spp. with helminths was observed in some HIV-patients in Kinshasa, DRC, suggesting the need for improved epidemiological surveillance and hygiene to reduce transmission and level of infection.
The complex picture of Cryptosporidium transmission in recent years continues to emerge because of the increase use of molecular tools for diagnosis. In a study that cuts across four countries (Kenya, Malawi, Brazil, and Vietnam), four genotypes of Cryptosporidium were identified; C. parvum human genotypes, C. parvum bovine genotype, C. meleagridis genotype, and Cryptosporidium muris genotype from HIV patients were documented. This finding is significant because the broad range of these species confirms that they are environmentally ubiquitous. The natural reservoirs of these species are believed to be poultry, rodents, and cattle. However, the results are difficult to interpret because of the small number of cases identified. In addition, when HIV-infected individuals are perceived to be more likely to have zoonotic genotypes than non-HIV infected individuals, there is close human proximity with animals. This is a common scenario in most parts of rural settings in Africa. Subsequently, Cranendonk et al. assessed the importance of C. parvum and I. belli (actually designated Cystoisopora belli) infections as a cause of diarrhea among HIV/AIDS patients with 11% positive for Cryptosporidium. Infection was significantly higher in the cohort with diarrhea than in those without diarrhea, confirming the dominance of C. parvum infection which is significantly associated with diarrhea among population studied. Similar study in Madagascar also associated C. parvum and I.belli with diarrhea in AIDS patients but one of the limitation of the study was the non-characterization of the various species to ascertain the molecular epidemiology of the parasite. Future studies must consider a holistic approach to understand the molecular epidemiology of cryptosporidiosis in most of these areas.
In Limpopo Province, South Africa, seroprevalence of Cryptosporidium in HIV-infected adults and local University students confirmed the high prevalence of Cryptosporidium (75.3%) in HIV-infected individuals compared with student volunteers (32.8%). Suggesting that there is possibility of widespread exposure to the parasite in both groups and the underlying risk factor maybe the source of drinking water. Numerous opportunistic infections occur in HIV-infected patients as result of the downregulation of the immune system. To determine if there was any correlation between Cryptosporidium infection and other IP associated with diarrhea, Samie et al. reported corroborated the coexistence of Cryptosporidium and IP among HIV patients using loop-mediated isothermal amplification technique. Cryptosporidium spp. was found in 26.4%, which supports data from previous reports that Cryptosporidium and other IP are associated with diarrhea.,, Principal risk factors seem to coincide with residing in rural areas, consumption of nonpiped water, close contact with cow dung and anthroponotic transmission. Moreover, another study implicated farm animals as a source of human infection and Cryptosporidium from calves to humans was reported in 18 cases among 82 farm workers and 207 households. The study identified C. parvum (75%) in farm workers, household members (60%) and in calves (62%). Of the positive calves, 62% were infected with C. parvum indicating zoonotic transmission among the workers. Similarly, Mtapuri-Zinyowera et al. reported enteric IP coexisting with Cryptosporidium. C. parvum (7.6%) and C. cayetanensis (22.1%) showed a remarkable high rate of infection among HIV patients. Interestingly, 11 (36.6%) water bodies had protozoan parasites associated with diarrhea including C. parvum (3.3%). This water sources used by rural populace are not treated and therefore pose a risk for acquiring such organisms. This emphasizes the need for early detection and treatment of such infection in HIV-infected patients to reduce morbidity. Some of the prevalence and molecular epidemiology studies are summarized in [Table 1].
|Table 1: Some studies on prevalence rates of Cryptosporidium species in Southern African countries|
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| Animal Cryptosporidiosis in Southern African Countries|| |
Humans acquire Cryptosporidium infection through several transmission routes, such as anthroponotic (persontoperson transmission), zoonotic (animal transmission), or contaminated fomites, or foodborne or water contaminated with infected feces. The different role of animals in the transmission of human cryptosporidiosis in most developing countries requires adequate attention. In several studies in Southern Africa, most of the Cryptosporidium strains found to have infected humans are nonzoonotic; however, C. hominis, C. parvum, C. meleagridis, Ctenocephalides felis, Ctenocephalides canis, Cryptosporidium cuniculus. Chlamydia suis, C. muris, Cryptosporidium Andersoni, and Cryptosporidium ubiquitum have been associated with human diseases.,
These infectious agents pose one of the greatest threats to endangered species and a greater risk of transmission from humans to wildlife. They should be considered a public health concern in tourism. An increased anthropogenic impact on primate populations may result in high level of interaction between parasite, humans, and primates. To assess such impact in the Central African Republic, a study evaluated the influence of close contact with humans and potential transmission zoonotic protists in western lowland Gorillas (Gorilla gorilla gorilla) on microsporidia, Cryptosporidium and Giardia infections at different stages of the habituation, humans, and other wildlife. Corynebacterium bovis was detected in gorilla and humans, and only G. intestinalis subgroup AII in gorilla. In other wild and domestic animals, E. cuniculi, G. intestinalis assemblage E and C. muris TS03 were identified, suggesting high potential of zoonotic transmission The observed possibility of human–gorilla transmission of parasites emphasized need to improve on hygiene where there is an increased human–gorilla contact. Moreover, Cryptosporidium is a persistent challenge to livestock production. Recently, molecular epidemiology in Madagascar confirmed C. suis as the dominant species infecting humans, cattle, pigs, and rodents. The broad species range of C. suis and lack of common cattle species (C. parvum and C. andersoni) are astonishing. Therefore, transmission of C. suis maybe widespread in humans and cattle than previously envisaged in the studied environment. Other studies have also documented the presence of Cryptosporidium in various animals in Madagascar and Malawi., The prevalence rate was between 5.6%-37% and occurrence was throughout all seasons. Species identified were C. hominis, C. parvum, C. bovis, and/or C. ryanae from various animals, indicating the presence of zoonotic and probably anthroponotic transmission in Malawi.
Moreover, studies have considered cattle a common source of zoonotic cryptosporidiosis since they are considered as major host of C. parvum worldwide. However, C. andersoni, C. bovis, and C. ryannae also infect cattle, and their occurrence is related to the age of the host. Recently, Abu Samra et al. identified C. parvum from elephant (Loxodonta africana), buffalo (Syncerus caffer), and impala (Aepyceros melampus) from Kruger National Park with different prevalence rates. This demonstrated transmission between wildlife, domestic animals and humans should be of concern. Within the same Park, Abu Samra et al. identified C. andersoni in calves, C. ubiquitum in impala and C. bovis in one buffalo. C. ubiquitum has been reported to infect a wide array of hosts; wild and domesticated ruminants, rodents, carnivores, primates, and humans. Supporting previous studies on zoonotic transmission of Cryptosporidium in South Africa, the parasite was detected in cats and dogs. High level of infection was found more in stray dogs and cats which could have public health implication for humans and other animals. There is abundant evidence that zoonotic transmission of this parasite in animals and game reserves have serious implication in public health where tourism is considered.,,,,,,,,,,,,,, Nevertheless, understanding how environmental conditions and social and behavioral factors influence transmission is important.
The paper on ecology and epidemiology of Cryptosporidium in humans, nonhuman primates, and livestock confirms a complex molecular epidemiology between humans, baboons and a subset of chimpanzees infected with C. hominis subtype IfA12G2; another subset of chimpanzees was infected with C. xiaoi. Despite the high degree of habitat overlap established, the dominance of C. hominis subtype IfA12G2 among humans and nonhuman primates suggest cross-species and anthropozoonotic transmission in the system studied. Cryptosporidiosis causes enormous economic losses in animals' husbandry and livestock production. To obtain information on the occurrence of cryptosporidiosis in lamb and other livestock, and the potential zoonotic role of Cryptosporidium isolates, C. suis and C. parvum was identified in lambs and goat kids which could be a potential reservoir for human infection in Zambia. Recently, Cryptosporidium and Giardia were found in pigs from Zambia and 6.9% had a mixed infection. Presence of the pathogens may have potential zoonotic effects on humans and public health hazard in Zambia and elsewhere.
| Cryptosporidium Spp. in Water Sources of Southern African Countries|| |
Water is the major transmission route of Cryptosporidium and Giardia, the oocysts and cysts can resist and remain infective for long periods and resistant to conventional water treatment.,,,,,,,,,, The infective dose required by Cryptosporidium and Giardia varies according to authors.,, Nevertheless, most chemicals used for disinfection are not practical outside the laboratory and high concentrations that significantly reduce oocyst infectivity are either very expensive or quite toxic. In several countries in Southern Africa, unavailability of good drinking water is still a major challenge and common sources of drinking water in rural settings include rivers, reservoirs, canals, and low land reservoirs. Farm animals, humans, and wild animals are considered major contributors of Cryptosporidium and Giardia (oo) cysts contamination of surface water. Few reports have indicated that dual infection with Giardia cysts and Cryptosporidium oocyst(s) in all types of water tested including surface water, sewage, or treated effluents in South Africa.,, The two pathogens were found in a significant percentage. The drawback of some of these small-scale studies was that molecular characterization was not performed to determine exposure route. River water has been identified as a significant source of Cryptosporidium and other pathogens in most developing countries.,, Emphasizing that detection of both organisms in water sources is vital because of its public health implications. Dungeni and Momba assessed the effectiveness of four wastewater treatments plants of the Gauteng Province and identified C. parvum and G. intestinalis as major pathogens. Thus, confirming that both pathogens are ubiquitous in the influents and raises serious public health concern in rural and urban settings.
The World Health Organization estimated that 80% of all diarrheal cases and illnesses are attributed to unsafe water supply and sanitation. In rural and some urban settings such as those found in Zimbabwe and other African countries, drinking water is obtained from protected and unprotected water bodies representing important risk factors for waterborne gastroenteritis., Proper identification of pathogens is extremely important, not only because of clinical implications but for epidemiological purposes. It is important that more studies be undertaken in these countries because there is glaring evidence of the inadequate source of good drinking water and the need to implement systemic monitoring programs for both protozoa in Southern Africa region. Cryptosporidiosis is a major infectious agent associated with diarrhea in most low-income countries; however, there are insufficient data on Cryptosporidium species contamination of water sources and the need to assess species/genotypes identification in respect of human infection.
| Conclusion|| |
The major obstacles to human health in most developing countries are associated unsafe water, poor sanitation, and personal hygiene. All these factors facilitate the transmission of Cryptosporidium and other protozoans associated with diarrhea in Southern Africa. Couple with the high prevalence of HIV/AIDS in this region, and the emergence of intestinal opportunistic parasites in humans should be of concern to public health officials and scientists. Despite the importance of cryptosporidiosis in childhood health, there is still lack of adequate attention to transmission of this parasite in Southern Africa. Considering the poor sanitation, hygiene, close proximity with animals, contamination of water bodies, effective control measures are needed to reduce the prevalence of this pathogen and other protozoans associated with diarrhea. Evidence has shown from the review that both anthroponotic and zoonotic transmission is common. There is still a wide gap in understanding the transmission route and molecular epidemiology in Southern Africa in relation to a population infected with HIV/AIDS and inadequate source of drinking water. Molecular characterization of most identified species is still lacking because facilities for such are inadequate or unavailable in most countries. The absence of effective drug(s) or vaccine to cure or prevent cryptosporidiosis is still a challenge. It is appropriate to search for alternative drugs of choice by considering isolation of bioactive compounds from medicinal plants for novel lead drugs. Although molecular studies have enhanced our understanding of Cryptosporidium transmission in developed countries, however, there are insufficient data in Southern Africa.
The authors are grateful to the Directorate of Research Development, University of the Free State for Postdoctoral Fellowship of Dr. Ojuromi. We also acknowledge the support from the management of Lagos State University, Ojo, Lagos, Nigeria. The authors also wish to acknowledge the efforts of Prof. Olga Matos of Unidade de Parasitologia Medica, Institute de Hygiene e Medicina Tropical, Universidade Nova de Lisboa, Portugal, for her thoughtful comments during the review of this manuscript.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
CIA World Fact Book; 2013.
Mandeville KL, Krabshuis J, Ladep NG, Mulder CJ, Quigley EM, Khan SA, et al.
Gastroenterology in developing countries: Issues and advances. World J Gastroenterol 2009;15:2839-54.
Bryce J, Boschi-Pinto C, Shibuya K, Black RE; WHO Child Health Epidemiology Reference Group. WHO estimates of the causes of death in children. Lancet 2005;365:1147-52.
Obimbo EM, Mbori-Ngacha DA, Ochieng JO, Richardson BA, Otieno PA, Bosire R, et al.
Predictors of early mortality in a cohort of human immunodeficiency virus type 1-infected African children. Pediatr Infect Dis J 2004;23:536-43.
UNAIDS. Global AIDS Update; 2016. p. 1-13.
Bandali S, Thomas C, Hukin E, Matthews Z, Mathai M, Ramachandran Dilip T, et al.
Maternal death surveillance and response systems in driving accountability and influencing change. Int J Gynaecol Obstet 2016;135:365-71.
Checkley W, White AC Jr. Jaganath D, Arrowood MJ, Chalmers RM, Chen XM, et al.
Areview of the global burden, novel diagnostics, therapeutics, and vaccine targets for Cryptosporidium
. Lancet Infect Dis 2015;15:85-94.
Korpe PS, Haque R, Gilchrist C, Valencia C, Niu F, Lu M, et al.
Natural history of cryptosporidiosis in a longitudinal study of slum-dwelling Bangladeshi children: Association with severe malnutrition. PLoS Negl Trop Dis 2016;10:e0004564.
UNICEF-WHO-The World Bank: Joint child malnutrition estimates-Levels and trends. 2013
Checkley W, Epstein LD, Gilman RH, Black RE, Cabrera L, Sterling CR, et al.
Effects of Cryptosporidium parvum
infection in Peruvian children: Growth faltering and subsequent catch-up growth. Am J Epidemiol 1998;148:497-506.
Mølbak K, Andersen M, Aaby P, Højlyng N, Jakobsen M, Sodemann M, et al. Cryptosporidium
infection in infancy as a cause of malnutrition: A community study from Guinea-Bissau, West Africa. Am J Clin Nutr 1997;65:149-52.
Agnew DG, Lima AA, Newman RD, Wuhib T, Moore RD, Guerrant RL, et al.
Cryptosporidiosis in Northeastern Brazilian children: Association with increased diarrhea morbidity. J Infect Dis 1998;177:754-60.
Mondal D, Haque R, Sack RB, Kirkpatrick BD, Petri WA Jr. Attribution of malnutrition to cause-specific diarrheal illness: Evidence from a prospective study of preschool children in Mirpur, Dhaka, Bangladesh. Am J Trop Med Hyg 2009;80:824-6.
Ryan U, Fayer R, Xiao L. Cryptosporidium
species in humans and animals: Current understanding and research needs. Parasitology 2014;141:1667-85.
Ryan U, Paparini A, Tong K, Yang R, Gibson-Kueh S, O'Hara A, et al. Cryptosporidium huwi
n. sp. (Apicomplexa: Eimeriidae) from the guppy (Poecilia reticulata
). Exp Parasitol 2015;150:31-5.
Ryan UM, Xiao L. Taxonomy and molecular taxonomy. In: Cacciò SM, Widmer G, editors. Cryptosporidium
: Parasite and Disease. New York, USA: Springer; 2014. p. 1-22.
Ryan U, Hijjawi N. New developments in Cryptosporidium
research. Int J Parasitol 2015;45:367-73.
Bulled N, Singer M, Dillingham R. The syndemics of childhood diarrhoea: A biosocial perspective on efforts to combat global inequities in diarrhoea-related morbidity and mortality. Glob Public Health 2014;9:841-53.
Snelling WJ, Xiao L, Ortega-Pierres G, Lowery CJ, Moore JE, Rao JR, et al.
Cryptosporidiosis in developing countries. J Infect Dev Ctries 2007;1:242-56.
Muchiri JM, Ascolillo L, Mugambi M, Mutwiri T, Ward HD, Naumova EN, et al.
Seasonality of Cryptosporidium
oocyst detection in surface waters of Meru, Kenya as determined by two isolation methods followed by PCR. J Water Health 2009;7:67-75.
Samie A, Guerrant RL, Barrett L, Bessong PO, Igumbor EO, Obi CL, et al.
Prevalence of intestinal parasitic and bacterial pathogens in diarrhoeal and non-diarroeal human stools from Vhembe district, South Africa. J Health Popul Nutr 2009;27:739-45.
Wegayehu T, Adamu H, Petros B. Prevalence of Giardia
duodenalis and Cryptosporidium
species infections among children and cattle in North Shewa Zone, Ethiopia. BMC Infect Dis 2013;13:419.
Moss JA, Gordy J, Snyder RA. Effective concentration and detection of Cryptosporidium
, and the microsporidia from environmental matrices. J Pathog 2014;2014:408204.
Dillingham RA, Lima AA, Guerrant RL. Cryptosporidiosis: Epidemiology and impact. Microbes Infect 2002;4:1059-66.
Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, et al.
Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the global enteric multicenter study, GEMS): A prospective, case-control study. Lancet 2013;382:209-22.
Lima AA, Samie A, Guerrant RL. Cryptosporidiosis. In: Guerrant RL, Walker DH, Weller PF, editors. Tropical Infectious Diseases. Philadelphia, Pa: Elsevier-Churchill Livingstone; 2011. p. 640-63.
Huang DB, Chappell C, Okhuysen PC. Cryptosporidiosis in children. Semin Pediatr Infect Dis 2004;15:253-9.
Kirkpatrick BD, Noel F, Rouzier PD, Powell JL, Pape JW, Bois G, et al.
Childhood cryptosporidiosis is associated with a persistent systemic inflammatory response. Clin Infect Dis 2006;43:604-8.
Creek TL, Kim A, Lu L, Bowen A, Masunge J, Arvelo W, et al.
Hospitalization and mortality among primarily nonbreastfed children during a large outbreak of diarrhea and malnutrition in Botswana, 2006. J Acquir Immune Defic Syndr 2010;53:14-9.
Areeshi M, Dove W, Papaventsis D, Gatei W, Combe P, Grosjean P, et al. Cryptosporidium
species causing acute diarrhoea in children in Antananarivo, Madagascar. Ann Trop Med Parasitol 2008;102:309-15.
Amadi B, Kelly P, Mwiya M, Mulwazi E, Sianongo S, Changwe F, et al.
Intestinal and systemic infection, HIV, and mortality in Zambian children with persistent diarrhea and malnutrition. J Pediatr Gastroenterol Nutr 2001;32:550-4.
Lunn PG. The impact of infection and nutrition on gut function and growth in childhood. Proc Nutr Soc 2000;59:147-54.
Petri WA Jr. Miller M, Binder HJ, Levine MM, Dillingham R, Guerrant RL, et al.
Enteric infections, diarrhea, and their impact on function and development. J Clin Invest 2008;118:1277-90.
Humphrey JH. Child undernutrition, tropical enteropathy, toilets, and handwashing. Lancet 2009;374:1032-5.
McKay S, Gaudier E, Campbell DI, Prentice AM, Albers R. Environmental enteropathy: New targets for nutritional interventions. Int Health 2010;2:172-80.
Guerrant RL, DeBoer MD, Moore SR, Scharf RJ, Lima AA. The impoverished gut – A triple burden of diarrhoea, stunting and chronic disease. Nat Rev Gastroenterol Hepatol 2013;10:220-9.
Ngure FM, Reid BM, Humphrey JH, Mbuya MN, Pelto G, Stoltzfus RJ, et al.
Water, sanitation, and hygiene (WASH), environmental enteropathy, nutrition, and early child development: Making the links. Ann N
Y Acad Sci 2014;1308:118-28.
Brown J, Cumming O, Bartram J, Cairncross S, Ensink J, Holcomb D, et al.
Acontrolled, before-and-after trial of an urban sanitation intervention to reduce enteric infections in children: Research protocol for the Maputo sanitation (MapSan) study, Mozambique. BMJ Open 2015;5:e008215.
Ullrich R, Zeitz M, Heise W, L'age M, Höffken G, Riecken EO, et al.
Small intestinal structure and function in patients infected with human immunodeficiency virus (HIV): Evidence for HIV-induced enteropathy. Ann Intern Med 1989;111:15-21.
Kotler DP, Francisco A, Clayton F, Scholes JV, Orenstein JM. Small intestinal injury and parasitic diseases in AIDS. Ann Intern Med 1990;113:444-9.
Hunter PR, Nichols G. Epidemiology and clinical features of Cryptosporidium
infection in immunocompromised patients. Clin Microbiol Rev 2002;15:145-54.
Hunter PR. Climate change and waterborne and vector-borne disease. J Appl Microbiol 2003;94 Suppl:37S-46S.
Navin TR, Weber R, Vugia DJ, Rimland D, Roberts JM, Addiss DG, et al.
Declining CD4+T-lymphocyte counts are associated with increased risk of enteric parasitosis and chronic diarrhea: Results of a 3-year longitudinal study. J Acquir Immune Defic Syndr Hum Retrovirol 1999;20:154-9.
Florez AC, Gracia DA, Moncada L, Beltran M. Prevalence of microsporidia and other intestinal parasites with HIV infection. Bogota Biomedica 2003; 23: 274–82.
Hadfield SJ, Robinson G, Elwin K, Chalmers RM. Detection and differentiation of Cryptosporidium
spp. in human clinical samples by use of real-time PCR. J Clin Microbiol 2011;49:918-24.
Lobo ML, Augusto J, Antunes F, Ceita J, Xiao L, Codices V, et al. Cryptosporidium
duodenalis, Enterocytozoon bieneusi
and other intestinal parasites in young children in Lobata province, democratic republic of São Tomé and Principe. PLoS One 2014;9:e97708.
Rowe JS, Shah SS, Motlhagodi S, Bafana M, Tawanana E, Truong HT, et al.
An epidemiologic review of enteropathogens in Gaborone, Botswana: Shifting patterns of resistance in an HIV endemic region. PLoS One 2010;5:e10924.
Alexander KA, Herbein J, Zajac A. The occurrence of Cryptosporidium
infections among patients reporting diarrheal disease in Chobe District, Botswana. Adv Infect Dis 2012;2:143-7.
Alexander KA, Blackburn JK. Overcoming barriers in evaluating outbreaks of diarrheal disease in resource poor settings: Assessment of recurrent outbreaks in Chobe district, Botswana. BMC Public Health 2013;13:775.
Goldfarb DM, Steenhoff AP, Pernica JM, Chong S, Luinstra K, Mokomane M, et al.
Evaluation of anatomically designed flocked rectal swabs for molecular detection of enteric pathogens in children admitted to hospital with severe gastroenteritis in Botswana. J Clin Microbiol 2014;52:3922-7.
GBD 2013 Mortality and Causes of Death Collaborators. Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990-2013: A systematic analysis for the global burden of disease study 2013. Lancet 2015;385:117-71.
Morse TD, Nichols RA, Grimason AM, Campbell BM, Tembo KC, Smith HV, et al.
Incidence of cryptosporidiosis species in paediatric patients in Malawi. Epidemiol Infect 2007;135:1307-15.
Peng MM, Meshnick SR, Cunliffe NA, Thindwa BD, Hart CA, Broadhead RL, et al.
Molecular epidemiology of cryptosporidiosis in children in Malawi. J Eukaryot Microbiol 2003;50 Suppl:557-9.
Ghaffari S, Kalantari N. A multi-locus study of Cryptosporidium
parasites isolated from patients living in Iran, Malawi, Nigeria, the United Kingdom, and Vietnam. Iran J Parasitol 2014;9:79-89.
Stehr-Green JK, McCaig L, Remsen HM, Rains CS, Fox M, Juranek DD, et al.
Shedding of oocysts in immunocompetent individuals infected with Cryptosporidium
. Am J Trop Med Hyg 1987;36:338-42.
Edelman MJ, Oldfield EC. Severe cryptosporidiosis in an immunocompetent host. Arch Intern Med 1988;148:1873-4.
Steele AD, Gove E, Meewes PJ. Cryptosporidiosis in white patients in South Africa. J Infect 1989;19:281-5.
van den Ende GM. Cryptosporidiosis among black children in hospital in South Africa. J Infect 1986;13:25-30.
Fripp PJ, Bothma MT. Cryptosporidium
associated with diarrhoeal at GaRankuwa Hospital. South Afr Epidemiol Infect1987;2:45-7.
Berkowitz FE, Vallabh W, Buqwana A, Heney C. Cryptosporidiosis in black South African children. S Afr Med J 1988;74:272-3.
Walters IN, Miller NM, van den Ende J, Dees GC, Taylor LA, Taynton LF, et al.
Outbreak of cryptosporidiosis among young children attending a day-care centre in Durban. S Afr Med J 1988;74:496-9.
Jarmey-Swan BI, Howgrave-Graham AR. Ubiquity of water-borne pathogens, Cryptosporidium
in KwaZulu-Natal populations. Water South Afr 2001;27:57-64.
Leav BA, Mackay MR, Anyanwu A, O' Connor RM, Cevallos AM, Kindra G, et al.
Analysis of sequence diversity at the highly polymorphic Cpgp40/15 locus among Cryptosporidium
isolates from human immunodeficiency virus-infected children in South Africa. Infect Immun 2002;70:3881-90.
Samie A, Bessong PO, Obi CL, Sevilleja JE, Stroup S, Houpt E, et al. Cryptosporidium
species: Preliminary descriptions of the prevalence and genotype distribution among school children and hospital patients in the Venda region, Limpopo province, South Africa. Exp Parasitol 2006;114:314-22.
Abu Samra N, Thompson PN, Jori F, Frean J, Poonsamy B, du Plessis D, et al.
Genetic characterization of Cryptosporidium
spp. in diarrhoeic children from four provinces in South Africa. Zoonoses Public Health 2013;60:154-9.
McLauchlin J, Amar C, Pedraza-Díaz S, Nichols GL. Molecular epidemiological analysis of Cryptosporidium
spp. in the United Kingdom: Results of genotyping Cryptosporidium
spp. in 1,705 fecal samples from humans and 105 fecal samples from livestock animals. J Clin Microbiol 2000;38:3984-90.
Tiangtip R, Jongwutiwes S. Molecular analysis of Cryptosporidium
species isolated from HIV-infected patients in Thailand. Trop Med Int Health 2002;7:357-64.
Cama VA, Bern C, Sulaiman IM, Gilman RH, Ticona E, Vivar A, et al. Cryptosporidium
species and genotypes in HIV-positive patients in lima, Peru. J Eukaryot Microbiol 2003;50 Suppl 1:531-3.
Matos O, Alves M, Xiao L, Cama V, Antunes F. Cryptosporidium felis
and C. meleagridis
in persons with HIV, Portugal. Emerg Infect Dis 2004;10:2256-7.
Dlamini MS, Nkambule SJ, Grimason AM. First report of cryptosporidiosis in paediatric patients in Swaziland. Int J Environ Health Res 2005;15:393-6.
Moyo SJ, Gro N, Matee MI, Kitundu J, Myrmel H, Mylvaganam H, et al.
Age specific aetiological agents of diarrhoea in hospitalized children aged less than five years in Dar es Salaam, Tanzania. BMC Pediatr 2011;11:19.
Cegielski JP, Msengi AE, Dukes CS, Mbise R, Redding-Lallinger R, Minjas JN, et al.
Intestinal parasites and HIV infection in Tanzanian children with chronic diarrhea. AIDS 1993;7:213-21.
Pedersen SH, Wilkinson AL, Andreasen A, Warhurst DC, Kinung'hi SM, Urassa M, et al. Cryptosporidium
prevalence and risk factors among mothers and infants 0 to 6 months in rural and semi-rural Northwest Tanzania: A prospective cohort study. PLoS Negl Trop Dis 2014;8:e3072.
Houpt ER, Bushen OY, Sam NE, Kohli A, Asgharpour A, Ng CT, et al.
Short report: Asymptomatic Cryptosporidium hominis
infection among human immunodeficiency virus-infected patients in Tanzania. Am J Trop Med Hyg 2005;73:520-2.
Moodley D, Jackson TF, Gathiram V, van den Ende J. Cryptosporidium
infections in children in Durban. Seasonal variation, age distribution and disease status. S Afr Med J 1991;79:295-7.
Nchito M, Kelly P, Sianongo S, Luo NP, Feldman R, Farthing M, et al.
Cryptosporidiosis in urban Zambian children: An analysis of risk factors. Am J Trop Med Hyg 1998;59:435-7.
Kelly P, Davies SE, Mandanda B, Veitch A, McPhail G, Zulu I, et al.
Enteropathy in Zambians with HIV related diarrhoea: Regression modelling of potential determinants of mucosal damage. Gut 1997;41:811-6.
Siwila J, Phiri IG, Enemark HL, Nchito M, Olsen A. Seasonal prevalence and incidence of Cryptosporidium
spp. and Giardia
duodenalis and associated diarrhoea in children attending pre-school in Kafue, Zambia. Trans R Soc Trop Med Hyg 2011;105:102-8.
Gumbo T, Sarbah S, Gangaidzo IT, Ortega Y, Sterling CR, Carville A, et al.
Intestinal parasites in patients with diarrhea and human immunodeficiency virus infection in Zimbabwe. AIDS 1999;13:819-21.
Dwivedi KK, Prasad G, Saini S, Mahajan S, Lal S, Baveja UK, et al.
Enteric opportunistic parasites among HIV infected individuals: Associated risk factors and immune status. Jpn J Infect Dis 2007;60:76-81.
Assefa S, Erko B, Medhin G, Assefa Z, Shimelis T. Intestinal parasitic infections in relation to HIV/AIDS status, diarrhea and CD4 T-cell count. BMC Infect Dis 2009;9:155.
Omoruyi B, Matongo F, Nkwetshana NT, Green E, Clarke AM, Ndip RN, et al.
Environmental and demographic risk factors associated with the prevalence of Cryptosporidium
infection in the Alice rural settlements of the Eastern Cape province of South Africa: A pilot study. Rev Environ Health 2011;26:127-33.
Abarca V K, López Del P
J, Peña D A, López G JC. Pet ownership and health status of pets from immunocompromised children, with emphasis in zoonotic diseases. Rev Chilena Infectol 2011;28:205-10.
Nel ED, Rabie H, Goodway J, Cotton MF. A retrospective study of cryptosporidial diarrhea in a region with high HIV prevalence. J Trop Pediatr 2011;57:289-92.
Wumba R, Enache-Angoulvant A, Develoux M, Mulumba A, Mulumba PM, Hennequin C, et al.
Prevalence of opportunistic digestive parasitic infections in Kinshasa, democratic republic of Congo. Results of a preliminary study in 50 AIDS patients. Med Trop (Mars) 2007;67:145-8.
Wumba R, Longo-Mbenza B, Mandina M, Odio WT, Biligui S, Sala J, et al.
Intestinal parasites infections in hospitalized AIDS patients in Kinshasa, democratic republic of Congo. Parasite 2010;17:321-8.
Wumba R, Longo-Mbenza B, Menotti J, Mandina M, Kintoki F, Situakibanza NH, et al.
Epidemiology, clinical, immune, and molecular profiles of microsporidiosis and cryptosporidiosis among HIV/AIDS patients. Int J Gen Med 2012;5:603-11.
Gatei W, Greensill J, Ashford RW, Cuevas LE, Parry CM, Cunliffe NA, et al.
Molecular analysis of the 18S rRNA gene of Cryptosporidium
parasites from patients with or without human immunodeficiency virus infections living in Kenya, Malawi, Brazil, the United Kingdom, and Vietnam. J Clin Microbiol 2003;41:1458-62.
Cranendonk RJ, Kodde CJ, Chipeta D, Zijlstra EE, Sluiters JF. Cryptosporidium parvum
and isospora belli infections among patients with and without diarrhoea. East Afr Med J 2003;80:398-401.
Clavero AO, Verdú ME, Pemán J, Dario R, Gobernado M. Human intestinal infection due to coccidia in Mozambique: Two cases. Acta Trop 1999;72:25-9.
Bartelt LA, Sevilleja JE, Barrett LJ, Warren CA, Guerrant RL, Bessong PO, et al.
High anti-Cryptosporidium parvum
IgG seroprevalence in HIV-infected adults in Limpopo, South Africa. Am J Trop Med Hyg 2013;89:531-4.
Samie A, Makuwa S, Mtshali S, Potgieter N, Thekisoe O, Mbati P, et al.
Parasitic infection among HIV/AIDS patients at bela-bela clinic, Limpopo province, South Africa with special reference to Cryptosporidium
. Southeast Asian J Trop Med Public Health 2014;45:783-95.
Cegielski JP, Ortega YR, McKee S, Madden JF, Gaido L, Schwartz DA, et al. Cryptosporidium
, and Cyclospora
infections in pediatric and adult patients with diarrhea in Tanzania. Clin Infect Dis 1999;28:314-21.
Tarimo DS, Killewo JZ, Minjas JN, Msamanga GI. Prevalence of intestinal parasites in adult patients with enteropathic AIDS in North-Eastern Tanzania. East Afr Med J 1996;73:397-9.
Siwila J, Phiri IG, Vercruysse J, Goma F, Gabriel S, Claerebout E, et al.
Asymptomatic cryptosporidiosis in Zambian dairy farm workers and their household members. Trans R Soc Trop Med Hyg 2007;101:733-4.
Mtapuri-Zinyowera S, Ruhanya V, Midzi N, Berejena C, Chin'ombe N, Nziramasanga P, et al.
Human parasitic protozoa in drinking water sources in rural Zimbabwe and their link to HIV infection. Germs 2014;4:86-91.
Xiao L. Molecular epidemiology of cryptosporidiosis: An update. Exp Parasitol 2010;124:80-9.
Nichols RA, Connelly L, Sullivan CB, Smith HV. Identification of Cryptosporidium
species and genotypes in Scottish raw and drinking waters during a one-year monitoring period. Appl Environ Microbiol 2010;76:5977-86.
Sak B, Petrzelkova KJ, Kvetonova D, Mynarova A, Shutt KA, Pomajbikova K, et al.
Long-term monitoring of microsporidia, Cryptosporidium
infections in Western Lowland gorillas (Gorilla gorilla gorilla
) at different stages of habituation in Dzanga Sangha protected areas, central African republic. PLoS One 2013;8:e71840.
Bodager JR, Parsons MB, Wright PC, Rasambainarivo F, Roellig D, Xiao L, et al.
Complex epidemiology and zoonotic potential for Cryptosporidium suis
in rural Madagascar. Vet Parasitol 2015;207:140-3.
Rasambainarivo FT, Gillespie TR, Wright PC, Arsenault J, Villeneuve A, Lair S, et al.
Survey of Giardia
in lemurs from the Ranomafana National Park, Madagascar. J Wildl Dis 2013;49:741-3.
Banda Z, Nichols RA, Grimason AM, Smith HV. Cryptosporidium
infection in non-human hosts in Malawi. Onderstepoort J Vet Res 2009;76:363-75.
Santín M, Fayer R. Intragenotypic variations in the Cryptosporidium
sp. cervine genotype from sheep with implications for public health. J Parasitol 2007;93:668-72.
Abu Samra N, Jori F, Samie A, Thompson P. The prevalence of Cryptosporidium
spp. oocysts in wild mammals in the Kruger National Park, South Africa. Vet Parasitol 2011;175:155-9.
Abu Samra N, Jori F, Xiao L, Rikhotso O, Thompson PN. Molecular characterization of Cryptosporidium
species at the wildlife/livestock interface of the Kruger National Park, South Africa. Comp Immunol Microbiol Infect Dis 2013;36:295-302.
Samie SA, Tsipa MA, Bessong P. The epidemiology of Cryptosporidium
in cats and dogs in the Thohoyandou region, South Africa. South Afr J Microbiol Res 2013;7:2510-8.
Jiang J, Alderisio KA, Xiao L. Distribution of Cryptosporidium
genotypes in storm event water samples from three watersheds in New York. Appl Environ Microbiol 2005;71:4446-54.
Fayer R, Santín M, Macarisin D. Cryptosporidium ubiquitum
n. sp. in animals and humans. Vet Parasitol 2010;172:23-32.
Matovelo JA, Landsverk T, Amaya Posada G. Cryptosporidiosis in Tanzanian goat kids: Scanning and transmission electron microscopic observations. Acta Vet Scand 1984;25:322-6.
Mtambo MM, Sebatwale JB, Kambarage DM, Muhairwa AP, Maeda GE, Kusiluka LJ, et al.
Prevalence of Cryptosporidium
spp. oocysts in cattle and wildlife in Morogoro region, Tanzania. Prev Vet Med 1997;31:185-90.
Kusiluka LJ, Karimuribo ED, Mdegela RH, Luoga EJ, Munishi PK, Mlozi MR, et al
. Prevalence and impact of water-borne zoonotic pathogens in water, cattle and humans in selected villages in Dodoma Rural and Bagamoyo districts, Tanzania. Phys Chem Earth 2005;30:818-25.
Swai ES, French NP, Karimuribo ED, Fitzpatrick JL, Bryant MJ, Kambarage DM, et al.
Prevalence and determinants of Cryptosporidium
spp. Infection in smallholder dairy cattle in Iringa and Tanga regions of Tanzania. Onderstepoort J Vet Res 2007;74:23-9.
Swai ES, Schoonman L. Investigation into the prevalence of Cryptosporidium
infection in calves among small-holder dairy and traditional herds in Tanzania. Vet Med Int 2010;2010:676451.
Chang'a JS, Robertson LJ, Mtambo MM, Mdegela RH, Løken T, Reksen O, et al.
Unexpected results from large-scale cryptosporidiosis screening study in calves in Tanzania. Ann Trop Med Parasitol 2011;105:513-9.
Gonzalez-Moreno O, Hernandez-Aguilar RA, Piel AK, Stewart FA, Gracenea M, Moore J, et al.
Prevalence and climatic associated factors of Cryptosporidium
sp. Infections in savanna chimpanzees from Ugalla, Western Tanzania. Parasitol Res 2013;112:393-9.
Fayer R, Morgan U, Upton SJ. Epidemiology of Cryptosporidium
: Transmission, detection and identification. Int J Parasitol 2000;30:1305-22.
Gómez MS, Torres J, Gracenea M, Fernandez-Morán J, Gonzalez-Moreno O. Further report on Cryptosporidium
in Barcelona Zoo mammals. Parasitol Res 2000;86:318-23.
Lonsdorf E, Travis DA, Rudicell RS, Gillespie TR, Salzer J, O'Donnell C, et al
. Observational health assessments of the Gombe chimpanzees: Correlating clinical signs with diagnosed infections. 32nd
Conference of the American Society of Primatologists. San Diego, California; 2009.
Parsons MB, Travis D, Lonsdorf EV, Lipende I, Roellig DM, Collins A, et al.
Epidemiology and molecular characterization of Cryptosporidium
spp. In humans, wild primates, and domesticated animals in the Greater Gombe Ecosystem, Tanzania. PLoS Negl Trop Dis 2015;9:e0003529.
Geurden T, Goma FY, Siwila J, Phiri IG, Mwanza AM, Gabriel S, et al.
Prevalence and genotyping of Cryptosporidium
in three cattle husbandry systems in Zambia. Vet Parasitol 2006;138:217-22.
Atwill ER, Johnson E, Klingborg DJ, Veserat GM, Markegard G, Jensen WA, et al.
Age, geographic, and temporal distribution of fecal shedding of Cryptosporidium parvum
oocysts in cow-calf herds. Am J Vet Res 1999;60:420-5.
Goma FY, Geurden T, Siwila J, Phiri IG, Gabriel S, Claerebout E, et al
. The prevalence and molecular characterisation of Cryptosporidium
spp. in small ruminants in Zambia. Small Ruminant Res 2007;72:77-80.
Siwila J, Mwape KE. Prevalence of Cryptosporidium
spp. and Giardia
duodenalis in pigs in Lusaka, Zambia. Onderstepoort J Vet Res 2012;79:E1-5.
Fayer R. Cryptosporidium: A water-borne zoonotic parasite. Vet Parasitol 2004;126:37-56.
Nwachcuku N, Gerba CP. Emerging waterborne pathogens: Can we kill them all? Curr Opin Biotechnol 2004;15:175-80.
Cacciò SM, Ryan U. Molecular epidemiology of giardiasis. Mol Biochem Parasitol 2008;160:75-80.
Lobo ML, Xiao L, Antunes F, Matos O. Occurrence of Cryptosporidium and Giardia
genotypes and subtypes in raw and treated water in Portugal. Lett Appl Microbiol 2009;48:732-7.
Sunnotel O, Lowery CJ, Moore JE, Dooley JS, Xiao L, Millar BC, et al.
Cryptosporidium. Lett Appl Microbiol 2006;43:7-16.
Garcia LS. Diagnostic Medical Parasitology. 5th
ed. Washington DC: ASM Press; 2007. p. 57-75.
Adam RD. Biology of Giardia lamblia
. Clin Microbiol Rev 2001;14:447-75.
Chappell CL, Okhuysen PC, Langer-Curry R, Widmer G, Akiyoshi DE, Tanriverdi S, et al. Cryptosporidium hominis
: Experimental challenge of healthy adults. Am J Trop Med Hyg 2006;75:851-7.
Kfir R, Hilner C, du Preez M, Bateman B. Studies on the prevalence of Giardia
cysts and oocysts in South African water. Water Sci Technol 1995;31:435-8.
Gericke M, Bateman B, Rapholo F, Mashakana J, Majaray V, Hilner C, et al
. Occurrence of protozoan parasites in South African source and treated water. WRC Report No. 451/1/95. Pretoria, South Africa: Water Research Commission; 1995.
Grundlingh M, De Wet CM. The search for Cryptosporidium
oocysts and Giardia
cysts in source water used for purification. Proceedings of the 2004 Water Institute of Southern Africa (WISA) Biennial Conference; 2004. p. 22-7.
Momba MN, Osode AN, Sibewu M. The Impact of inadequate wastewater treatment on the receiving water bodies-Case study: Buffalo City and Nkonkobe Municipalities of the Eastern Cape. Water South Afr 2006;32:687-92.
Clarke ME, Giddings CW, Mcevoy JM. Sources of Cryptosporidium
in a rural watershed. International Workshop on Opportunistic Protists. Boston MA; May, 2008.
Pennil CC, Clark ME, Giddings CW, Mcevoy JM. Sources of Cryptosporidium
in a Rural Watershed. National Water Quality Conference, Sparks, Nevada; 2008.
Dungeni M, Momba MN. The abundance of Cryptosporidium
spp. in treated effluents produced by four wastewater treatment plants in the Gauteng Province of South Africa. Water South Afr 2010;36:425-31.
Kelly P, Baboo KS, Ndubani P, Nchito M, Okeowo NP, Luo NP, et al.
Cryptosporidiosis in adults in Lusaka, Zambia, and its relationship to oocyst contamination of drinking water. J Infect Dis 1997;176:1120-3.
Ashbolt NJ. Microbial contamination of drinking water and disease outcomes in developing regions. Toxicology 2004;198:229-38.
Mor SM, Tzipori S. Cryptosporidiosis in children in sub-Saharan Africa: A lingering challenge. Clin Infect Dis 2008;47:915-21.
Dr. Anofi Omotayo T. Ashafa
Faculty of Natural and Agricultural Sciences, University of The Free State, Qwaqwa Campus, Private Bag X13, Phuthaditjhaba, 9866
Source of Support: None, Conflict of Interest: None