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Cryptosporidium and Giardia in Africa: current and future challenges
Parasites & Vectors volume 10, Article number: 195 (2017)
Cryptosporidium and Giardia are important causes of diarrhoeal illness. Adequate knowledge of the molecular diversity and geographical distribution of these parasites and the environmental and climatic variables that influence their prevalence is important for effective control of infection in at-risk populations, yet relatively little is known about the epidemiology of these parasites in Africa. Cryptosporidium is associated with moderate to severe diarrhoea and increased mortality in African countries and both parasites negatively affect child growth and development. Malnutrition and HIV status are also important contributors to the prevalence of Cryptosporidium and Giardia in African countries. Molecular typing of both parasites in humans, domestic animals and wildlife to date indicates a complex picture of both anthroponotic, zoonotic and spill-back transmission cycles that requires further investigation. For Cryptosporidium, the only available drug (nitazoxanide) is ineffective in HIV and malnourished individuals and therefore more effective drugs are a high priority. Several classes of drugs with good efficacy exist for Giardia, but dosing regimens are suboptimal and emerging resistance threatens clinical utility. Climate change and population growth are also predicted to increase both malnutrition and the prevalence of these parasites in water sources. Dedicated and co-ordinated commitments from African governments involving “One Health” initiatives with multidisciplinary teams of veterinarians, medical workers, relevant government authorities, and public health specialists working together are essential to control and prevent the burden of disease caused by these parasites.
Infectious diarrhoea is a major cause of death in children under 5 years old in Africa . Unsafe water supplies and inadequate levels of sanitation and hygiene increase the transmission of diarrhoeal diseases and despite ongoing efforts to enhance disease surveillance and response, many African countries face challenges in accurately identifying, diagnosing and reporting infectious diseases due to the remoteness of communities, lack of transport and communication infrastructures, and a shortage of skilled health care workers and laboratory facilities to ensure accurate diagnosis .
The enteric protozoan parasites Cryptosporidium and Giardia are important causes of diarrhoeal disease [3–6], with Cryptosporidium the most common diarrhoea-causing protozoan parasite worldwide . The recent Global Enteric Multicenter Study (GEMS) and other studies to identify the aetiology and population-based burden of paediatric diarrhoeal disease in sub-Saharan Africa, revealed that Cryptosporidium is second only to rotavirus as a contributor to moderate-to-severe diarrhoeal disease during the first 5 years of life . It has been estimated that 2.9 million Cryptosporidium-attributable cases occur annually in children aged < 24 months in sub-Saharan Africa  and infection is associated with a greater than two-fold increase in mortality in children aged 12 to 23 months .
Giardia duodenalis is the species infecting mammals, including humans, and is estimated to cause 2.8 × 108 cases of intestinal diseases per annum globally [10, 11], with a higher prevalence in developing countries including Africa . Most infections are self-limited but recurrences are common in endemic areas. Chronic infection can lead to weight loss and malabsorption  and is associated with stunting (low height for age), wasting (low weight for height) and cognitive impairment in children in developing countries [13–15]. Furthermore, acute giardiasis may disable patients for extended periods and can elicit protracted post-infectious syndromes, including irritable bowel syndrome and chronic fatigue .
In Africa, GEMS reported that Giardia was not significantly positively associated with moderate-to-severe diarrhoea . However, experimental challenge studies unequivocally document that some strains of G. duodenalis can cause diarrhoea in healthy adult volunteers [17, 18], and a recent systematic review and meta-analysis of endemic paediatric giardiasis concluded that there is an apparently paradoxical association with protection from acute diarrhoea, yet an increased risk of persistent diarrhoea .
In addition to diarrhoea, both protozoans have been associated with abdominal distension, vomiting, fever and weight loss in mostly children and HIV/AIDS individuals [20–29]. Malnutrition, which impairs cellular immunity, is an important risk factor for cryptosporidiosis  and Cryptosporidium infection in children is associated with malnutrition, persistent growth retardation, impaired immune response and cognitive deficits [31–33]. The mechanism by which Cryptosporidium affects child growth seems to be associated with inflammatory damage to the small intestine . Undernutrition (particularly in children) is both a sequela of, and a risk factor for, cryptosporidiosis [33, 35–40]. For both parasites, breast-feeding is associated with protection against clinical cryptosporidiosis and giardiasis [19, 41–43], even though it does not generally prevent acquisition of Giardia infection or chronic carriage .
Currently 31 Cryptosporidium species are considered valid [44–48]. Among these, more than 20 Cryptosporidium spp. and genotypes have been reported in humans, although C. parvum and C. hominis remain the most common [6, 48, 49]. Giardia duodenalis consists of eight assemblages (A to H) with different host specificities; Assemblage A in humans, livestock and other mammals; B in humans, primates and some other mammals, C and D in dogs and other canids; E mainly in hoofed animals including cattle, sheep and goats and more recently in humans; F in cats and humans; G in rats; and H in marine mammals [50, 51].
Infection may be acquired through direct contact with infected persons (person-to-person transmission) or animals (zoonotic transmission) and ingestion of contaminated food (foodborne transmission) and water (waterborne transmission) [6, 11, 52]. Numerous studies have demonstrated that respiratory cryptosporidiosis may occur commonly in both immunocompromised and immunocompetent individuals and that Cryptosporidium may also be transmitted via respiratory secretions . Several studies also suggest that flies may play an important role in the mechanical transmission of Cryptosporidium and Giardia including human infectious species [54–64].
Relatively little is known about the epidemiology of cryptosporidiosis and giardiasis in African countries [65, 66], although a recent review of Cryptosporidium in Africa focussed on the epidemiology and transmission dynamics . The purpose of this review is to compare the prevalence and molecular epidemiology of both Cryptosporidium and Giardia in Africa, with a focus on current and future challenges and to develop recommendations for better control of these important parasites.
Diagnosis and prevalence of Cryptosporidium and Giardia in Africa
Morphological identification of Giardia and Cryptosporidium (oo)cysts in faecal samples by microscopy either directly or after the application of stains including Acid Fast, Lugol’s iodine and immunofluorescent antibody staining are the most widely used methods for diagnosis of these parasites in Africa due to their relatively low cost (Table 1). In-house and commercial immunoassays including copro-antigen tests kits, Crypto-Giardia immuno-chromatographic dipstick kits, faecal antigen ELISA kits ImmunoCard STAT and CoproStrip™ Cryptosporidium are also widely used either alone or in combination with other techniques for research purposes (Table 1). Studies on Cryptosporidium and Giardia have mostly been in children aged 0–16 years, at primary schools, with or without gastrointestinal symptoms or community-based studies, while others have involved different groups of individuals including both HIV/AIDS-positive and negative patients (Table 1). There are also studies on food handlers or vendors and high-risk individuals in close contact with animals such as national park staff, people living close to national parks, and farmers and their households as well as solid waste workers . As a result of the different diagnostic methods utilised, the prevalence of Cryptosporidium and Giardia in different African studies varies widely (Table 1), with prevalence of < 1% in children and adults and > 72% in diarrhoeic patients reported for Cryptosporidium and < 1% in children and HIV-positive and negative patients and > 62% in primary school children (Table 1).
The immune status of the host, both innate and adaptive immunity, has a major impact on the severity of cryptosporidiosis and giardiasis and their prognosis [3, 50, 51, 68]. With both parasites, immunocompetent individuals typically experience self-limiting diarrhoea and transient gastroenteritis lasting up to 2 weeks and recover without treatment, suggesting an efficient host anti-Cryptosporidium/Giardia immune responses [3, 68]. With cryptosporidiosis, immunocompromised individuals including HIV/AIDS patients (not treated with antiretroviral therapy) often suffer from intractable diarrhoea, which can be fatal . HIV status is an important host risk factor particularly for cryptosporidiosis and although Cryptosporidium is an important pathogen regardless of HIV-prevalence , HIV-positive children are between three and eighteen times more likely to have Cryptosporidium than those who are HIV-negative [70–72]. The unfolding HIV/AIDS epidemic in African countries, with > 25 million adults and children infected with HIV/AIDS in 2015 , is a major contributor to the increased prevalence of cryptosporidiosis and giardiasis in Africa.
The impact of malnutrition usually falls mainly on children under 5 years of age  and malnutrition is an important risk factor for both diarrhoea and prolonged diarrhoea caused by Cryptosporidium and Giardia , with significantly higher rates of Cryptosporidium infection in malnourished children controlling for HIV status [33, 39, 74, 75].
Molecular detection and characterisation of Cryptosporidium and Giardia
Molecular tools for the detection and characterisation of these parasites are increasingly being used however, particularly for research purposes due to increased specificity and sensitivity and the ability to identify species [29, 76–81]. The most commonly used genotyping tools for Cryptosporidium in Africa are PCR and restriction fragment length polymorphism (RFLP) and/or sequence analysis of the 18S rRNA gene [23, 25, 28, 72, 82–103] (Table 1), although some studies have relied on the Cryptosporidium oocyst wall protein (COWP) gene [26, 82, 92, 100, 104–108], which is not as reliable as the 18S locus at identifying and differentiating Cryptosporidium species . Subtyping of Cryptosporidium has been conducted mainly at the glycoprotein 60 (gp60) gene locus [23, 26, 82, 93–95, 98, 100, 102, 108, 110–115] (Table 2) while others targeted the heat shock protein 70 (HSP70) gene [91, 92, 100, 116–118]. Genotyping of Giardia in Africa, has mainly been conducted using the triose-phosphate isomerase (tpi) gene, beta-giardin (bg) and glutamate dehydrogenase (gdh) genes, either alone or using a combination of two or three loci [80, 99, 103, 119–124] (see Tables 1, 3 and 4).
Risk factor analysis have associated a higher prevalence of Cryptosporidium and/or Giardia with various factors including contact with animals and manure [25, 26, 125], the location of an individual such as living in villages versus cities, drinking underground or tap water [25, 26, 80], living in a household with another Cryptosporidium-positive person , and eating unwashed/raw fruit .
Precipitation is thought to be a strong seasonal driver for cryptosporidiosis in tropical countries [126, 127]. Many studies in Africa have reported a higher prevalence of Cryptosporidium during high rainfall seasons. For example, studies in Ghana (West Africa), Guinea-Bissau (West Africa), Tanzania (East Africa), Kenya (East Africa) and Zambia (southern Africa) have reported a higher prevalence of Cryptosporidium just before, or at the onset of the rainy season and a higher prevalence of Giardia in cool seasons in Tanzania [20, 72, 128]. However, other studies from Rwanda, Malawi, Kenya and South Africa have reported a higher prevalence of cryptosporidiosis at the end of rainy seasons and beginning of the drier months [129, 130]. Studies in Egypt (North Africa) reported a peak prevalence for both Cryptosporidium and Giardia during summer (drier months) with a second peak in winter for Giardia [131, 132]. It is possible that the apparent seasonality of human disease, is reflective of different transmission pathways, hosts, and/or Cryptosporidium and Giardia species in different locations. As climate change occurs, transmission patterns of many waterborne diseases may shift, and studies in African locations with unusual seasonality patterns will help inform our understanding of what climate change may bring.
Cryptosporidium and Giardia co-infections and co-infections with other pathogens have been observed in numerous studies in Africa [21, 129, 133–136]. In Kenya, polyparasitism was more common in patients with diarrhoea than those with single infections of intestinal parasites . Multiple infections could impact on the host’s response to infection, as synergistic interaction between co-infecting pathogens has been shown to enhance diarrhoea pathogenesis. For example, in Ecuador, South America, simultaneous infection with rotavirus and Giardia resulted in a greater risk of having diarrhoea than would be expected if the co-infecting organisms acted independently of one another .
Cryptosporidium and Giardia species reported in humans in Africa
Genotyping of Cryptosporidium species in Africa have identified at least 13 species and genotypes in humans including C. hominis, C. parvum, C. meleagridis, C. ubiquitum, C. viatorum, C. andersoni, C. bovis, C. canis, C. cuniculus, C. felis, C. muris, C. suis and C. xiaoi [23, 25, 26, 86, 97, 101, 102, 115, 139–142] (see Table 2).
Cryptosporidium hominis and C. parvum are the main species infecting humans [6, 143–145]. Out of the 56 molecular studies in African countries analysed, C. hominis was the most prevalent (2.4–100%) Cryptosporidium species in humans in 38 of the studies followed by C. parvum (3.0–100%) in 13 studies and C. meleagridis (75%) in one study, C. viatorum and C. hominis (40% each) in one study and a single species of C. muris, C. suis and C. viatorum in the remaining three studies (See Table 2).
Cryptosporidium meleagridis is also recognized as an important human pathogen in many African countries including Kenya, Cote d’Ivoire, Equatorial Guinea, Ethiopia, Malawi, Nigeria, South Africa, Tunisia and Uganda [23, 25, 70, 86, 89, 101, 106, 114, 129, 140, 141, 146–154]. In immunocompromised individuals, the prevalence of C. meleagridis can reach 75% (3/4 of samples typed) [23, 25, 101, 146, 147, 151, 152], but also 75% (9/12 of samples typed) in immunocompetent individuals [86, 106, 114, 141, 149, 153, 155, 156]. In comparison, the prevalence of C. meleagridis in the developed world is ~1% .
Other Cryptosporidium species including C. viatorum, C. canis, C. muris, C. felis, C. suis and C. xiaoi have been detected in immunocompromised individuals [23, 83, 139, 147] and C. andersoni, C. bovis, C. viatorum, C. canis, C. muris, C. felis and C. suis in immunocompetent individuals, particularly children [86, 95, 97, 103, 129, 141, 149, 153].
Subtyping studies of Cryptosporidium to date supports the dominance of anthroponotic transmission in African countries, despite close contact with farm animals. For example, a study conducted in children in the rural Ashanti region of Ghana reported that the human-to-human transmitted C. hominis subtype families Ia, Ib, Id and Ie made up 58.0% of all Cryptosporidium isolates typed, and within C. parvum, the largely anthroponotically transmitted subtypes families IIc and IIe, were detected in 42.0% of samples typed . High levels of subtype diversity are also frequently reported, which is a common finding in developing countries and is thought to reflect intensive and stable anthroponotic Cryptosporidium transmission [6, 23, 89, 96, 98, 115, 141]. Similarly, another study in Kenyan children identified C. hominis subtypes in the majority of positives typed (82.8%), while the C. parvum IIc subtype family was identified in 18.8% of positives  (Table 2). To date, seven C. hominis subtype families (Ia, Ib, Id, Ie, If and Ih) have been identified in African countries (Table 2).
The mainly anthroponotically transmitted C. parvum IIc subtype family is the predominant subtype in sub-Saharan Africa, including Malawi, Nigeria, South Africa, and Uganda [87, 89, 98, 115, 141, 148, 152, 157]. However, it is important to note that the IIc subtype family has been detected in hedgehogs in Europe [158–160], suggesting potential zoonotic transmission.
In addition to the C. parvum IIc and the rarer anthroponotically transmitted IIe subtype family, a range of additional C. parvum subtype families (IIa, IIb, IId, IIg, Iii, IIh and IIm) have been identified in humans (Table 2). The C. parvum subtype family IIm, which was discovered in Nigeria , also appears to be anthroponotically transmitted, as it has not been identified in animals. High occurrences of zoonotic C. parvum subtype families (IIa and IId) have however been detected in some studies in Egypt, Ethiopia and Tunisia [23, 82, 95, 108, 140]. Few subtyping studies have been conducted on C. meleagridis isolates with C. meleagridis subtype IIIdA4 identified in humans in South Africa .
Recently a gp60 subtyping assay has been developed for C. viatorum , the only species that to date has been found exclusively in humans. A single subtype family, XVa, was identified containing multiple alleles (XVaA3a-XVaA3f) . A single case of XVaA3b originating in Kenya has been identified and nine samples from Ethiopia belonged to XVaA3d; however, this subtype is not a strictly African subtype as the same subtype was also identified in a United Kingdom patient with a history of traveling to Barbados . Currently no animal reservoir has been identified for C. viatorum, but extensive studies of animals in the same areas where the human infections originated are required to clarify whether animal reservoirs exist.
The relative clinical impact of C. hominis and C. parvum in African communities is poorly defined. In a study in children under 15 years in Ghana, C. hominis infection was mainly associated with diarrhoea whereas C. parvum infection was associated with both diarrhoea and vomiting . A study in Tanzania reported that C. hominis was the predominant species and was associated with a longer duration of symptoms, a higher rate of asymptomatic infection, and a lower CD4 cell count versus C. parvum-infected patients (P < 0.05) . However, another study in Uganda reported that the vast majority of children presenting with diarrhoea lasting for 31 days or longer were HIV-positive and were infected with isolates belonging to the C. parvum subtype family Iii, followed by the C. hominis subtype Ie. The C. parvum IIc and IIg and C. hominis Ia, Ie, and Id subtype families were found in children with diarrhoea lasting for 21 days or less .
Relatively few Giardia genotyping studies have been conducted in Africa, however available reports reveal that five G. duodenalis assemblages (A, B, C, E and F) have been identified in humans (Table 3). In Africa, Assemblage B was the most prevalent among typed samples (19.5–100%) in 18 out of 28 studies reviewed (Table 3) with Assemblage A the dominant assemblage (1.4–100%) in the remaining 10 studies [96, 122, 163–167] (see Table 3). Although many studies have reported that Giardia is not associated with severe diarrhoea , one study reported that the prevalence of G. duodenalis Assemblage A was higher among children with vomiting and abdominal pain . Assemblage C was detected in an adult immunocompromised male suffering from bladder cancer and diarrhoea in Egypt  and Assemblage F was reported in six diarrhoeal and one asymptomatic individual in Ethiopia . In that study, four of the identified Assemblage F isolates were mixed infections with Assemblage A. Assemblage E has been reported in humans in three separate studies in Egypt with a prevalence of up to 62.5% in one study population [80, 168, 169]. Subtyping studies in Africa have identified subassemblages AI, AII, BIII, BIV and various novel subassemblages (Table 3).
Cryptosporidium and Giardia in domesticated animals in Africa
In Africa, Cryptosporidium and Giardia have been reported in several domesticated animal species including cattle, sheep, goats, farmed buffalo, horses, poultry (chicken and turkey), pigs, cultured tilapia (fish) and dogs [26, 84, 93, 94, 97, 111, 123, 170–173]. However, the majority of research has been conducted on cattle. Prevalence ranging from < 1% in calves  to > 86% in calves  have been reported for Cryptosporidium and < 6%  to > 30%  prevalence for Giardia in adult cattle and calves, respectively. As with most studies, the prevalence of Cryptosporidium was greater in young animals (1 day to 3 months) than older ones. Age, source of drinking water and diarrhoea has been associated with Cryptosporidium prevalence in cattle [26, 118, 174]. For example, in a study in Egypt, calves watered with canal or underground water were at a higher risk of infection than calves watered with tap water .
Cryptosporidium parvum, C. ryanae, C. bovis and C. andersoni are the most common species detected in cattle (Bos taurus and Bos indicus), although C. hominis, C. suis and Cryptosporidium deer-like genotype have also been reported [26, 84, 90, 95, 97, 110, 112, 113, 118, 174, 176, 177]. Younger calves had a higher occurrence of C. bovis and C. ryanae while C. parvum seems to be dominant in pre-weaned calves [85, 112].
Although little research has been done in other domesticated animals, C. ryanae, C. bovis and C. parvum have been reported in farmed buffalos [95, 111, 113], C. xiaoi, C. bovis and C. suis in sheep [102, 113, 117, 178] and C. xiaoi and C. parvum in goats [102, 117] (Table 5). In addition, C. parvum and C. suis have been identified in pigs , C. erinacei in horses  and C. canis in dogs . Cryptosporidium meleagridis was identified in both turkeys and chickens [93, 178] and C. baileyi has been identified in chickens . All the species reported in domesticated animals, except for C. ryanae and C. baileyi, have been identified in humans from Africa [23, 25, 26, 97, 101, 102, 115, 139–142] (see Table 2), suggesting that domestic animals may act as zoonotic reservoirs for human infections. Humans working closely with farmed animals especially calves are known to be more at risk of zoonotic infection with C. parvum and may excrete oocysts without showing clinical symptoms and act as a source of infection for household members .
Subtyping of C. parvum from animals at the gp60 locus identified C. parvum subtypes IIa and IId, with IIaA15G1R1, IIaA15G2R1 and IIdA20G1 the most common [95, 110–113] (see Table 5). A unique subtype IIaA14G1R1r1b was also isolated from a calf in Egypt . Cryptosporidium erinacei subtype XIIIa was found in horses from Algeria . In a study in rural Madagascar, peri-domestic rodents were found to be infected with Cryptosporidium rat genotype III, rat genotype IV, C. meleagridis, C. suis and 2 unknown genotypes .
Giardia duodenalis Assemblage E is the dominant species in ruminant livestock (cattle, farmed buffalo and goats) from the Central African Republic, Egypt, Rwanda, Tanzania and Uganda [80, 120, 122–124, 169, 175, 179]. Assemblage A (subtypes AI and AII) has been reported in goats, cattle, buffalos, ducks and chickens from Cote d’Ivoire, Egypt, Tanzania and Uganda and Assemblage B (BIV) and/or Assemblage A and B have been reported in goats, ducks and cattle from Cote d’Ivoire, and Tanzania [80, 106, 120, 123, 169, 175, 179]. Assemblage A was also identified in cultured tilapia and mullet (Tilapia nilotica and Mugil cephalus, respectively) from Egypt .
Cryptosporidium and Giardia in African wildlife
The majority of studies on Cryptosporidium and Giardia in African wildlife have been conducted in wildlife parks. These studies have included western lowland gorillas from the Lope National Park in Gabon , mountain gorillas from the Bwindi Impenetrable National Park in Uganda and the Volcanoes National Park in Rwanda [104, 124, 163, 181, 182], chimpanzees from Tanzania, elephants, buffalos and impalas from the Kruger National Park, South Africa [90, 183], olive baboons from the Bwindi Impenetrable National Park, Uganda  and bamboo lemurs and eastern rufous mouse lemurs from the Ranomafana National Park, Madagascar [97, 185]. In addition, Cryptosporidium oocysts and Giardia (oo)cysts together with other gastrointestinal parasites (Nasitrema attenuata, Zalophotrema spp. and Pholeter gasterophilus) were found in dolphins in Egypt, but no genotyping was conducted .
Cryptosporidium hominis was reported in olive baboons from Kenya and Tanzania and in lemurs from Madagascar, suggesting possible spill-back from humans. Cryptosporidium hominis and C. suis has been reported in chimpanzees from Tanzania and [97, 102, 187] and C. parvum was reported in gorillas from Uganda . Subtyping at the gp60 locus identified C. hominis subtypes IfA12G2 (the commonest), IbA9G3 and a novel subtype IiA14 in olive baboons and chimpanzees from Kenya and Tanzania, respectively [102, 187]. In wild ruminants, C. ubiquitum and C. bovis has been identified in forest buffalos and C. ubiquitum in Impala from South Africa . Cryptosporidium ubiquitum is considered an emerging zoonotic pathogen  and has been reported in humans in Africa in Nigeria [86, 141] and increasing human encroachment into wildlife-populated areas in Africa, is likely to increase zoonotic transmission.
Giardia duodenalis Assemblage A and B (subtypes BIII and BIV) have been reported in gorillas from Uganda and Rwanda, respectively [124, 163] and Assemblage B in usrine colobus monkey from Ghana  (Table 4), again suggesting spill-back. Giardia duodenalis cysts have been found in the faeces of other animals including grasscutters (Thryonomys swinderianus) , but no genotyping was done. Almost all the Cryptosporidium and Giardia species identified in wildlife are infectious to humans with potential for zoonosis or spill-back from humans to animals. For example, a high prevalence of cryptosporidiosis was reported in park staff members (21%) who had frequent contact with gorillas versus 3% disease prevalence in the local community in Uganda .
Waterborne and foodborne cryptosporidiosis and giardiasis in Africa
As Cryptosporidium and Giardia (oo)cysts are robust and resistant to environmental conditions, including disinfectants such as chlorine used in water treatment systems, numerous waterborne and foodborne outbreaks of human cryptosporidiosis and giardiasis have been reported, with Cryptosporidium and Giardia responsible for > 95% of outbreaks worldwide [192–202].
Relatively little is known about the presence and prevalence of Cryptosporidium and Giardia in food and water in Africa. Both parasites have been detected in food such as fresh fruits and vegetables in Ethiopia, Egypt, Ghana, Libya and Sudan [203–207], and Tiger nuts (Cyperus esculentus) from Ghana . Cryptosporidium was detected in 16.8% of reared black mussels (Mytilus galloprovincialis) in Mali . Cryptosporidium does not multiply in bivalves, but they can be an effective transmission vehicle for Cryptosporidium oocysts, especially within 24–72 h of contamination, with viable oocysts present in bivalves up to 7 days post infection . Cryptosporidium and Giardia (oo)cysts were identified from 34.3% and 2.0% of coins and 28.2% and 1.9% of bank notes (respectively) used by food-related workers in Alexandria, Egypt . As coins and banknotes are some of the objects most handled and exchanged by people, this raises the potential of parasite transmission even between countries.
In many rural African households, untreated water is used for various purposes such as bathing, cooking, drinking and swimming, often exposing them to waterborne Cryptosporidium and Giardia [212, 213]. More than 300 million people in sub-Saharan Africa have poor access to safe water, predisposing them to infections from waterborne pathogens, and cryptosporidial infections are known to be prevalent among communities which lack access to clean potable water supply [214–216]. Poverty is therefore a key limiting factor to accessing safe water. In many communities, particularly those in rural areas where the average income is ~ US$1 per person per day , individuals have limited access to privately owned water resources that provide safe water . This, coupled with inadequate water treatment, poor hygiene practices, drinking unboiled water and lack of education programmes, predisposes many rural African communities to cryptosporidiosis and giardiasis .
Cryptosporidium oocysts and Giardia cysts have been detected in a variety of African water sources including irrigation water in Burkina Faso , a stream, well, spring and lake in Cameroon [220, 221], wastewater in Côte d’Ivoire , packaged drinking water in Ghana [223–225], tap water, drinking water treatment plants, canals, tanks and swimming pools in Egypt [226–230]. They have also been detected in water sources (surface and well), treated water storage tanks and tap water in Ethiopia [231, 232], the Kathita and Kiina rivers and surface water in Kenya [233, 234], water from wells and the Kano river in Nigeria , the surface waters of the Vaal Dam system , treated and untreated effluents, sewage, drinking water and roof-harvested rainwater in South Africa [237–240]. In Tunisia, they have been detected in watersheds, treated, raw wastewater and sludge samples [241, 242], in Uganda, in natural and communal piped tap water from the Queen Elizabeth protected area , in piped water in Zambia [243, 244] and wells, springs, tap water and rivers in Zimbabwe .
Genotyping of Cryptosporidium and Giardia from these water sources identified C. parvum from the Kathita and Kiina rivers, C. parvum and C. andersoni in Muru regional surface waters (both in Kenya) , C. hominis and Giardia Assemblages A and B in sewage treatment plants from South Africa [238, 240]. C. hominis (subtypes IdA15G1, IaA27R3), C. parvum (subtypes IIaA21, IIcA5G3b), C. muris, C. andersoni, Giardia Assemblage A (subtypes A1 and AII), B and a novel Giardia subtype were isolated from treated, raw wastewater and sludge samples in Tunisia . In addition, C. parvum (subtypes IIaA15G2R1, IIaA17G2R1, IIaA18G3R1, IIaA20G2R1, IIaA21R1, IIaA21G2R1, IIcA5G3b), C. muris, C. andersoni, C. hominis (subtypes IaA26R3, IaA27R4, IdA14), C. ubiquitum, Cryptosporidium rat genotype IV, novel Cryptosporidium genotypes, C. meleagridis, avian genotype II, Giardia Assemblage A (subtypes AI and AII), Assemblages B and E were isolated from treated and raw wastewater plants and sludge samples, also from Tunisia . In the latter report, the most prevalent genotypes were Assemblage A (86.8%) and C. andersoni (41.2%) out of 99 Giardia and 114 Cryptosporidium-positive PCR products, respectively.
Treatment of cryptosporidiosis and giardiasis in Africa
Another contributing factor to the high prevalence and widespread distribution of Cryptosporidium and Giardia in Africa is the lack of treatment options. Currently no effective vaccine exists for Cryptosporidium and only one drug, nitazoxanide (NTZ, Alinia; Romark Laboratories, Tampa, Florida, USA), is available for use against Cryptosporidium. This drug, however, is currently not recommended for use in infants < 12 months of age, exhibits only moderate clinical efficacy in malnourished children and immunocompetent people, and none in immunocompromised individuals like people with HIV [246, 247]. In 2015, > 25 million adults and children were infected with HIV/AIDS in Africa , and the UN Food and Agriculture Organization estimates that 233 million people in sub-Saharan Africa were malnourished in 2014–6 . The ineffectiveness of nitazoxanide in HIV-positive individuals and the contribution of malnourishment to impaired immunity , means that nitazoxanide is ineffective against the most important target population in Africa. In individuals co-infected with HIV, antiretroviral therapy (ART) has been successful in controlling chronic diarrhoea and wasting due to cryptosporidiosis [27, 249, 250]. Currently, supportive care and ART (for HIV/AIDS patients) form the basis for treatment of cryptosporidiosis.
As with Cryptosporidium, a human vaccine for giardiasis is not available. Several classes of antimicrobial drugs are available for the treatment of giardiasis. The most commonly utilised worldwide are members of the 5-nitroimidazole (5-NI) family such as metronidazole and tinidazole. However, this first line therapy fails in up to 20% of cases and cross-resistance between different agents can occur , and resistance to all major antigiardial drugs has been reported . Albendazole is also effective in treating giardiasis [251, 253], although its efficacy varies markedly (25–90%), depending on the dosing regimen . Nitazoxanide has been shown to reduce symptom duration in individuals with giardiasis  and quinacrine, an old malaria drug, reportedly has 90% efficacy against giardiasis , but has potentially severe adverse effects, including a number of psychiatric and dermatologic manifestations . For Cryptosporidium, new classes of more effective drugs are a high priority and for Giardia, improvements in potency and dosing of currently available drugs, and the ability to overcome existing and prevent new forms of drug resistance, are priorities in antigiardial drug development .
The prohibitive cost of de novo drug development, estimated to be between $500 million and $2 billion per compound successfully brought to market , is another major limiting factor in the development of anti-cryptosporidial and anti-giardial drugs. Treatment of Cryptosporidium and Giardia in African countries, despite having a large target population, has a small market in the developed world and pharmaceutical companies are often hesitant to invest in costly de novo campaigns to develop new therapeutics for developing countries. Therefore, the primary challenge for further drug development is the underlying economics, as both parasitic infections are considered Neglected Diseases with low funding priority and limited commercial interest . For this reason, there has been a movement to ‘repurpose’ existing therapeutics for off-label applications, as repurposed drugs cost around 60% less to bring to market than drugs developed de novo . For example, drugs such as the human 3-hydroxy-3-methyl-glutaryl-coenzyme A (HMG-CoA) reductase inhibitor, itavastatin and auranofin (Ridaura®) were initially approved for the treatment of rheumatoid arthritis and have been shown to be effective against Cryptosporidium in vitro [259, 260], which holds promise for future anticryptosporidial drugs.
The impact of climate change and HIV status on cryptosporidiosis and giardiasis in Africa
Waterborne transmission is a major mode of transmission for both Cryptosporidium and Giardia. Climate change represents a major threat for access to safe drinking water in Africa which has more climate sensitive economies than any other continent . Increasingly variable rainfall patterns are likely to affect the supply of fresh water in Africa. Some regions in Africa have become drier during the last century (e.g. the Sahel)  and by the 2090s, climate change is likely to widen the area affected by drought, double the frequency of extreme droughts and increase their average duration six-fold . Climate change will also increase levels of malnutrition in Africa, as it will lead to changes in crop yield, higher food prices and therefore lower affordability of food, reduced calorie availability, and growing childhood malnutrition in Sub-Saharan Africa . Malnutrition in turn undermines the resilience of vulnerable populations to cryptosporidial and giardial infections, decreasing their ability to cope and adapt to the consequences of climate change.
Surface water concentrations of Cryptosporidium and Giardia in Africa are also expected to increase with increased population growth. The Global Waterborne Pathogen model for human Cryptosporidium emissions, predicts that while Cryptosporidium emissions in developing countries will decrease by 24% in 2050, in Africa, emissions to surface water will increase by up to 70% . Given the lack of treatment options, particularly for Cryptosporidium, high-level community awareness, policy formulations and regular surveillance are needed in order to limit the waterborne, zoonotic and anthroponotic transmission of Cryptosporidium and Giardia.
This cannot be achieved, however, unless there is a commitment from African governments to supply clean potable water, particularly to rural communities, improve sanitation by connecting the population to sewers and improve waste water treatment. Community programmes must be initiated to educate the people on water safety measures, personal hygiene and water treatment processes. The achievement of these goals hinges on the elimination of malnutrition and a significant reduction in HIV levels in African populations. The introduction of ART in HIV patients which partially restores the immune function has been important in reducing the prevalence of Cryptosporidium in HIV patients [266, 267]. Furthermore, it has been suggested that HIV protease inhibitors can act as antiparasitic drugs. For example, in experimental studies, the drugs indinavir, saquinavir, and ritonavir have been reported to have anti-Cryptosporidium spp. effects both in vitro and in vivo . However, most African government have not invested sufficient funds and resources to ensuring alleviation of malnutrition and HIV [261, 269] and many HIV-prevention services still do not reach most of those in need , largely due to under-staffing of, and the poor geographical distribution of available services for those in need.
Despite the millennium development goals target to reduce hunger by half by 2015, major failures have been recorded in Africa. Out of the > 800 million people still suffering from hunger in the world, over 204 million come from Sub-Saharan Africa. The situation is currently getting worse in this region as it moved from 170.4 million hungry people in 1990 to 204 million in 2002 . This increase has generally been attributed to poverty, illiteracy, ignorance, big family sizes, climate change, policy and corruption .
Cryptosporidium and Giardia are prevalent in both humans and animals in Africa with both anthroponotic and zoonotic transmission cycles. Cryptosporidium is unequivocally associated with moderate-to-severe diarrhoea in African children but further studies are required to determine if Giardia infections in early infancy are positively linked to moderate-to-severe diarrhoea, whether some paediatric hosts (e.g. more stunted) are more prone to develop persistent diarrhoea, whether Giardia decreases the risk of acute diarrhoea from other specific enteropathogens, and whether specific Giardia assemblages exhibit enhanced pathogenicity over other assemblages and subassemblages. Efforts in reducing HIV in African countries should focus on earlier identification of HIV, providing earlier access to ART and improved case management for HIV-infected individuals (particularly children) and reducing the cultural and social stigma directed at persons living with HIV/AIDS. “One Health” initiatives involving multidisciplinary teams of veterinarians, medical workers, relevant government authorities, water and sanitation engineers, water managers and public health specialists working together are essential for the control and prevention of cryptosporidiosis and giardiasis in African countries.
Acquired immunodeficiency virus syndrome
- bg :
Cryptosporidium oocyst wall protein
- ef1-α :
Elongation factor 1-alpha
Enzyme linked immunosorbent assay
- gdh :
Global enteric multicenter study
- gp60 :
Human immunodeficiency virus
Human 3-hydroxy-3-methyl-glutaryl-coenzyme A
Heat shock protein 70
Internal transcribed spacer
Loop-mediated isothermal amplification
Quantitative real-time polymerase chain reaction
Ribosomal deoxyribonucleic acid
Restriction fragment length polymorphism
Ribosomal ribonucleic acid
- tpi :
Triose phosphate isomerase
Thrombospondin-related adhesive protein
Walker CLF, Aryee MJ, Boschi-Pinto C, Black RE. Estimating diarrhea mortality among young children in low and middle income countries. PLoS One. 2012;7(1):e29151.
World Health Statistics. World Health Organisation, Geneva Switzerland. 2015. http://apps.who.int/iris/bitstream/10665/170250/1/9789240694439_eng.pdf. Accessed 25 Sept 2016.
Eckmann L. Mucosal defences against Giardia. Parasite Immunol. 2003;25(5):259–70.
Chalmers RM, Davies AP. Minireview: clinical cryptosporidiosis. Exp Parasitol. 2010;124(1):138–46.
Feng Y, Xiao L. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev. 2011;24(1):110–40.
Xiao L. Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol. 2010;124(1):80–9.
Diarrhoea: Why children are still dying and what can be done. World Health Organization/United Nations International Children’s Emergency Fund (WHO/UNICEF), Geneva/New York. 2009. http://apps.who.int/iris/bitstream/10665/44174/1/9789241598415_eng.pdf. Accesed 25 Sept 2016.
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(9888):209–22.
Sow SO, Muhsen K, Nasrin D, Blackwelder WC, Wu Y, Farag TH, et al. The burden of Cryptosporidium diarrheal disease among children < 24 months of age in moderate/high mortality regions of sub-Saharan Africa and South Asia, utilizing data from the Global Enteric Multicenter Study (GEMS). PLoS Negl Trop Dis. 2016;10(5):e0004729.
Lane S, Lloyd D. Current trends in research into the waterborne parasite Giardia. Crit Rev Microbiol. 2002;28(2):123–47.
Thompson RCA. The zoonotic significance and molecular epidemiology of Giardia and giardiasis. Vet Parasitol. 2004;126(1):15–35.
Thomas IV, Lewis J, Zweig AP, Tosh AK. An adolescent with chronic giardiasis mimicking anorexia nervosa. Int J Adolesc Med Health. 2014;26(2):293–5.
Berkman DS, Lescano AG, Gilman RH, Lopez SL, Black MM. Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study. Lancet. 2002;359(9306):564–71.
Nematian J, Gholamrezanezhad A, Nematian E. Giardiasis and other intestinal parasitic infections in relation to anthropometric indicators of malnutrition: a large, population-based survey of schoolchildren in Tehran. Ann Trop Med Parasitol. 2008;102(3):209–14.
Al-Mekhlafi HM, Al-Maktari MT, Jani R, Ahmed A, Anuar TS, Moktar N, et al. Burden of Giardia duodenalis infection and its adverse effects on growth of school children in rural Malaysia. PLoS Negl Trop Dis. 2013;7(10):e2516.
Hanevik K, Wensaas K-A, Rortveit G, Eide GE, Mørch K, Langeland N. Irritable bowel syndrome and chronic fatigue 6 years after Giardia infection: a controlled prospective cohort study. Clin Infect Dis. 2014;59(10):1394–400.
Rendtorff EC, Holt CJ. The experimental transmission of human intestinal protozoan parasites. IV. Attempts to transmit Endamoeba coli and Giardia lamblia cysts by water. Am J Hyg. 1954;60(3):327–38.
Nash TE, Herrington DA, Losonsky GA, Levine MM. Experimental human infections with Giardia lamblia. J Infect Dis. 1987;156(6):974–84.
Muhsen K, Levine MM. A systematic review and meta-analysis of the association between Giardia lamblia and endemic pediatric diarrhea in developing countries. Clin Infect Dis. 2012;55 Suppl 4:S271–S93.
Tumwine JK, Kekitiinwa A, Nabukeera N, Akiyoshi DE, Rich SM, Widmer G, et al. Cryptosporidium parvum in children with diarrhea in Mulago Hospital, Kampala, Uganda. Am J Trop Med Hyg. 2003;68(6):710–5.
Abdel-Messih IA, Wierzba TF, Abu-Elyazeed R, Ibrahim AF, Ahmed SF, Kamal K, et al. Diarrhea associated with Cryptosporidium parvum among young children of the Nile River Delta in Egypt. J Trop Pediatr. 2005;51(3):154–9.
Ignatius R, Gahutu JB, Klotz C, Steininger C, Shyirambere C, Lyng M, et al. High prevalence of Giardia duodenalis Assemblage B infection and association with underweight in Rwandan children. PLoS Negl Trop Dis. 2012;6(6):e1677.
Adamu H, Petros B, Zhang G, Kassa H, Amer S, Ye J, et al. Distribution and clinical manifestations of Cryptosporidium species and subtypes in HIV/AIDS patients in Ethiopia. PLoS Negl Trop Dis. 2014;8(4):e2831.
Ignatius R, Gahutu JB, Klotz C, Musemakweri A, Aebischer T, Mockenhaupt FP, et al. Detection of Giardia duodenalis Assemblage A and B isolates by immunochromatography in stool samples from Rwandan children. Clin Microbiol Infect. 2014;20(10):O783–O4.
Wanyiri JW, Kanyi H, Maina S, Wang DE, Steen A, Ngugi P, et al. Cryptosporidiosis in HIV/AIDS patients in Kenya: clinical features, epidemiology, molecular characterization and antibody responses. Am J Trop Med Hyg. 2014;91(2):319–28.
Helmy YA, Samson-Himmelstjerna GV, Nockler K, Zessin KH. Frequencies and spatial distributions of Cryptosporidium in livestock animals and children in the Ismailia province of Egypt. Epidemiol Infect. 2015;143(6):1208–18.
Mengist HM, Taye B, Tsegaye A. Intestinal parasitosis in relation to CD4 + T cells levels and anemia among HAART initiated and HAART naive pediatric HIV patients in a model ART center in Addis Ababa, Ethiopia. PLoS One. 2015;10(2):e0117715.
Wumba RD, Zanga J, Mbanzulu KM, Mandina MN, Kahindo AK, Aloni MN, et al. Cryptosporidium identification in HIV-infected humans. Experience from Kinshasa, the Democratic Republic of Congo. Acta Parasitol. 2015;60(4):638–44.
Breurec S, Vanel N, Bata P, Chartier L, Farra A, Favennec L, et al. Etiology and epidemiology of diarrhea in hospitalized children from low income country: a matched case-control study in Central African Republic. PLoS Negl Trop Dis. 2016;10(1):e0004283.
Gendrel D, Treluyer JM, Richard-Lenoble D. Parasitic diarrhea in normal and malnourished children. Fundam Clin Pharmacol. 2003;17(2):189–97.
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(1):149–52.
Guerrant DI, Moore SR, Lima AA, Patrick PD, Schorling JB, Guerrant RL. Association of early childhood diarrhea and cryptosporidiosis with impaired physical fitness and cognitive function four-seven years later in a poor urban community in northeast Brazil. Am J Trop Med Hyg. 1999;61(5):707–13.
Mondal D, Haque R, Sack RB, Kirkpatrick BD, Petri WA. 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(5):824–6.
Kirkpatrick BD, Daniels MM, Jean SS, Pape JW, Karp C, Littenberg B, et al. Cryptosporidiosis stimulates an inflammatory intestinal response in malnourished Haitian children. J Infect Dis. 2002;186(1):94–101.
MacFarlane DE, Horner-Bryce J. Cryptosporidiosis in wellnourished and malnourished children. Acta Paediatr. 1987;76(3):474–7.
Sallon S, Deckelbaum RJ, Schmid II, Harlap S, Baras M, Spira DT. Cryptosporidium, malnutrition, and chronic diarrhea in children. Am J Dis Child. 1988;142(3):312–5.
Checkley W, Gilman RH, Epstein LD, Suarez M, Diaz JF, Cabrera L, et al. Asymptomatic and symptomatic cryptosporidiosis: their acute effect on weight gain in Peruvian children. Am J Epidemiol. 1997;145(2):156–63.
Bushen OY, Kohli A, Pinkerton RC, Dupnik K, Newman RD, Sears CL, et al. Heavy cryptosporidial infections in children in northeast Brazil: comparison of Cryptosporidium hominis and Cryptosporidium parvum. Trans R Soc Trop Med Hyg. 2007;101(4):378–84.
Mondal D, Minak J, Alam M, Liu Y, Dai J, Korpe P, et al. Contribution of enteric infection, altered intestinal barrier function, and maternal malnutrition to infant malnutrition in Bangladesh. Clin Infect Dis. 2012;54(2):185–92.
Quihui-Cota L, Lugo-Flores CM, Ponce-Martínez JA, Morales-Figueroa GG. Cryptosporidiosis: a neglected infection and its association with nutritional status in school children in northwestern Mexico. J Infect Dev Ctries. 2015;9(08):878–83.
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(1):14–9.
Abdel-Hafeez EH, Belal US, Abdellatif MZM, Naoi K, Norose K. Breast-feeding protects infantile diarrhea caused by intestinal protozoan infections. Korean J Parasitol. 2013;51(5):519–24.
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(10):e3072.
Li X, Pereira MGC, Larsen R, Xiao C, Phillips R, Striby K, et al. Cryptosporidium rubeyi n. sp. (Apicomplexa: Cryptosporidiidae) in multiple Spermophilus ground squirrel species. Int J Parasitol Parasit Wildl. 2015;4(3):343–50.
Kvac M, Havrdova N, Hlaskova L, Dankova T, Kandera J, Jezkova J, et al. Cryptosporidium proliferans n. sp (Apicomplexa: Cryptosporidiidae): Molecular and biological evidence of cryptic species within gastric Cryptosporidium of mammals. PLoS One. 2016;11(1):e0147090.
Holubová N, Sak B, Horčičková M, Hlásková L, Květoňová D, Menchaca S, et al. Cryptosporidium avium n. sp. (Apicomplexa: Cryptosporidiidae) in birds. Parasitol Res. 2016;115(6):2243–51.
Costa J, Cruz C, Eiras JC, Saraiva A. Characterization of a Cryptosporidium scophthalmi-like isolate from farmed turbot (Scophthalmus maximus) using histological and molecular tools. Dis Aquat Organ. 2016 (In press).
Zahedi A, Paparini A, Jian F, Robertson I, Ryan U. Public health significance of zoonotic Cryptosporidium species in wildlife: Critical insights into better drinking water management. Int J Parasitol Parasit Wildl. 2016;5(1):88–109.
Ryan U, Xiao L. Taxonomy and molecular taxonomy. In: Cacciò SM, Widmer G, editors. Cryptosporidium: parasite and disease. Vienna: Springer; 2014. p. 3–41.
Cacciò SM, Thompson RCA, McLauchlin J, Smith HV. Unravelling Cryptosporidium and Giardia epidemiology. Trends Parasitol. 2005;21(9):430–7.
Ryan U, Cacciò SM. Zoonotic potential of Giardia. Int J Parasitol. 2013;43(12-13):943–56.
Burnet JB, Penny C, Ogorzaly L, Cauchie HM. Spatial and temporal distribution of Cryptosporidium and Giardia in a drinking water resource: implications for monitoring and risk assessment. Sci Total Environ. 2014;472:1023–35.
Sponseller JK, Griffiths JK, Tzipori S. The evolution of respiratory cryptosporidiosis: evidence for transmission by inhalation. Clin Microbiol Rev. 2014;27(3):575–86.
Graczyk TK, Fayer R, Knight R, Mhangami-Ruwende B, Trout JM, Da Silva AJ, et al. Mechanical transport and transmission of Cryptosporidium parvum oocysts by wild filth flies. Am J Trop Med Hyg. 2000;63(3):178.
Graczyk TK, Grimes BH, Knight R, Szostakowska B, Kruminis-Lozowska W, Racewicz M, et al. Mechanical transmission of Cryptosporidium parvum oocysts by flies. Wiad Parazytol. 2004;50(2):243.
Szostakowska B, Kruminis-Lozowska W, Racewicz M, Knight R, Tamang L, Myjak P, et al. Cryptosporidium parvum and Giardia lamblia recovered from flies on a cattle farm and in a landfill. Appl Environ Microbiol. 2004;70(6):3742–4.
Graczyk TK, Knight R, Tamang L. Mechanical transmission of human protozoan parasites by insects. Clin Microbiol Rev. 2005;18(1):128–32.
Conn DB, Weaver J, Tamang L, Graczyk TK. Synanthropic flies as vectors of Cryptosporidium and Giardia among livestock and wildlife in a multispecies agricultural complex. Vector Borne Zoonotic Dis. 2007;7(4):643–51.
Getachew S, Gebre-Michael T, Erko B, Balkew M, Medhin G. Non-biting cyclorrhaphan flies (Diptera) as carriers of intestinal human parasites in slum areas of Addis Ababa, Ethiopia. Acta Trop. 2007;103(3):186–94.
Fetene T, Worku N. Public health importance of non-biting cyclorrhaphan flies. Trans R Soc Trop Med Hyg. 2009;103(2):187–91.
Fetene T, Worku N, Huruy K, Kebede N. Cryptosporidium recovered from Musca domestica, Musca sorbens and mango juice accessed by synanthropic flies in Bahirdar, Ethiopia. Zoonoses Public Health. 2011;58(1):69–75.
El-Sherbini GT, Gneidy MR. Cockroaches and flies in mechanical transmission of medical important parasites in Khaldyia Village, El-Fayoum, Governorate. J Egypt Soc Parasitol. 2012;42(1):165–74.
Adenusi AA, Adewoga TOS. Human intestinal parasites in non-biting synanthropic flies in Ogun State, Nigeria. Travel Med Infect Dis. 2013;11(3):181.
Zhao Z, Dong H, Wang R, Zhao W, Chen G, Li S, et al. Genotyping and subtyping Cryptosporidium parvum and Giardia duodenalis carried by flies on dairy farms in Henan, China. Parasit Vectors. 2014;7:190.
Mor SM, Tzipori S. Cryptosporidiosis in children in sub-Saharan Africa: a lingering challenge. Clin Infect Dis. 2008;47(7):915–21.
Aldeyarbi HM, Abu El-Ezz NMT, Karanis P. Cryptosporidium and cryptosporidiosis: the African perspective. Environ Sci Pollut Res. 2016;23(14):13811–21.
Eassa SM, El-Wahab EWA, Lotfi SE, El Masry SA, Shatat HZ, Kotkat AM. Risk Factors associated with parasitic infection among municipality solid-waste workers in an Egyptian community. J Parasitol. 2016;102(2):214–21.
Ryan U, Zahedi A, Paparini A. Cryptosporidium in humans and animals - a one health approach to prophylaxis. Parasite Immunol. 2016;38:535–47.
Current WL, Garcia LS. Cryptosporidiosis. Clin Microbiol Rev. 1991;4(3):325–58.
Tumwine JK, Kekitiinwa A, Bakeera-Kitaka S, Ndeezi G, Downing R, Feng X, et al. Cryptosporidiosis and microsporidiosis in Ugandan children with persistent diarrhea with and without concurrent infection with the human immunodeficiency virus. Am J Trop Med Hyg. 2005;73(5):921–5.
Mbae CK, Nokes DJ, Mulinge E, Nyambura J, Waruru A, Kariuki S. Intestinal parasitic infections in children presenting with diarrhoea in outpatient and inpatient settings in an informal settlement of Nairobi, Kenya. BMC Infect Dis. 2013;13:243.
Tellevik MG, Moyo SJ, Blomberg B, Hjollo T, Maselle SY, Langeland N, et al. Prevalence of Cryptosporidium parvum/hominis, Entamoeba histolytica and Giardia lamblia among young children with and without diarrhea in Dar es Salaam, Tanzania. PLoS Negl Trop Dis. 2015;9(10):e0004125.
Anonymous. Food and Nutrition Handbook. Rome: World Food Programme; 2000.
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(5):550–4.
Moore SR, Lima NL, Soares AM, Oriá RB, Pinkerton RC, Barrett LJ, et al. Prolonged episodes of acute diarrhea reduce growth and increase risk of persistent diarrhea in children. Gastroenterology. 2010;139(4):1156–64.
Verweij JJ, Blange RA, Templeton K, Schinkel J, Brienen EAT, van Rooyen MAA, et al. Simultaneous detection of Entamoeba histolytica, Giardia lamblia, and Cryptosporidium parvum in fecal samples by using multiplex real-time PCR. J Clin Microbiol. 2004;42(3):1220–3.
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(4):314–22.
Moshira MFH, Abdel-Fattah HS, Rashed L. Real-time PCR/RFLP assay to detect Giardia intestinalis genotypes in human isolates with diarrhea in Egypt. J Parasitol. 2009;95(4):1000–4.
Elsafi SH, Al-Maqati TN, Hussein MI, Adam AA, Hassan MMA, Al Zahrani EM. Comparison of microscopy, rapid immunoassay, and molecular techniques for the detection of Giardia lamblia and Cryptosporidium parvum. Parasitol Res. 2013;112(4):1641–6.
Helmy YA, Klotz C, Wilking H, Krucken J, Nockler K, Von Samson-Himmelstjerna G, et al. Epidemiology of Giardia duodenalis infection in ruminant livestock and children in the Ismailia province of Egypt: insights by genetic characterization. Parasit Vectors. 2014;7(1):321.
Easton AV, Oliveira RG, O’Connell EM, Kepha S, Mwandawiro CS, Njenga SM, et al. Multi-parallel qPCR provides increased sensitivity and diagnostic breadth for gastrointestinal parasites of humans: field-based inferences on the impact of mass deworming. Parasit Vectors. 2016;9:38.
Adamu H, Petros B, Hailu A, Petry F. Molecular characterization of Cryptosporidium isolates from humans in Ethiopia. Acta Trop. 2010;115(1-2):77–83.
Akinbo FO, Okaka CE, Omoregie R, Dearen T, Leon ET, Xiao L. Molecular characterization of Cryptosporidium spp. in HIV-infected persons in Benin City, Edo State, Nigeria. Fooyin J Health Sci. 2010;2(3):85–9.
Ayinmode AB, Olakunle FB, Xiao L. Molecular characterization of Cryptosporidium spp. in native calves in Nigeria. Parasitol Res. 2010;107(4):1019–21.
Maikai BV, Umoh JU, Kwaga JKP, Lawal IA, Maikai VA, Cama V, et al. Molecular characterization of Cryptosporidium spp. in native breeds of cattle in Kaduna State, Nigeria. Vet Parasitol. 2011;178(3):241–5.
Molloy SF, Tanner CJ, Kirwan P, Asaolu SO, Smith HV, Nichols RAB, et al. Sporadic Cryptosporidium infection in Nigerian children: risk factors with species identification. Epidemiol Infect. 2011;139(6):946–54.
Ayinmode AB, Fagbemi BO, Xiao L. Molecular characterization of Cryptosporidium in children in Oyo State, Nigeria: implications for infection sources. Parasitol Res. 2012;110(1):479–81.
Nyamwange CI, Mkoji G, Mpoke S, Nyandieka HS. Cyptosporidiosis and its genotypes among children attending Moi Teaching and Referral Hospital in Eldoret, Kenya. East Afr Med J. 2012;89(1):11–9.
Samra NA, 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(2):154–9.
Samra NA, 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(3):295–302.
Amer S, Fayed M, Honma H, Fukuda Y, Tada C, Nakai Y. Multilocus genetic analysis of Cryptosporidium parvum from Egypt. Parasitol Res. 2010;107(5):1043–7.
Amer S, Harfoush M, He H. Molecular and phylogenetic analyses of Cryptosporidium spp. from dairy cattle in Egypt. J Egypt Soc Parasitol. 2010;40(2):349–66.
Baroudi D, Khelef D, Goucem R, Adjou KT, Adamu H, Zhang H, et al. Common occurrence of zoonotic pathogen Cryptosporidium meleagridis in broiler chickens and turkeys in Algeria. Vet Parasitol. 2013;196(3):334–40.
Laatamna AE, Wagnerova P, Sak B, Kvetonova D, Aissi M, Rost M, et al. Equine cryptosporidial infection associated with Cryptosporidium hedgehog genotype in Algeria. Vet Parasitol. 2013;197(1):350–3.
Helmy YA, Krucken J, Nockler K, von Samson-Himmelstjerna G, Zessin KH. Molecular epidemiology of Cryptosporidium in livestock animals and humans in the Ismailia province of Egypt. Vet Parasitol. 2013;193(1):15–24.
Lobo ML, Augusto J, Antunes F, Ceita J, Xiao LH, Codices V, et al. Cryptosporidium spp., Giardia duodenalis, Enterocytozoon bieneusi and other intestinal parasites in young children in Lobata province, Democratic Republic of São Tomé and Príncipe. PLoS One. 2014;9(5):e97708.
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(1):140–3.
Eibach D, Krumkamp R, Al-Emran HM, Sarpong N, Hagen RM, Adu-Sarkodie Y, et al. Molecular characterization of Cryptosporidium spp. among children in rural Ghana. PLoS Negl Trop Dis. 2015;9(3):e0003551.
Flecha MJ, Benavides CM, Tissiano G, Tesfamariam A, Cuadros J, Lucio A, et al. Detection and molecular characterisation of Giardia duodenalis, Cryptosporidium spp. and Entamoeba spp. among patients with gastrointestinal symptoms in Gambo hospital, Oromia Region, southern Ethiopia. Trop Med Int Health. 2015;20(9):1213–22.
Laatamna AE, Wagnerová P, Sak B, Květoňová D, Xiao L, Rost M, et al. Microsporidia and Cryptosporidium in horses and donkeys in Algeria: detection of a novel Cryptosporidium hominis subtype family (Ik) in a horse. Vet Parasitol. 2015;208(3):135–42.
Ojuromi OT, Duan L, Izquierdo F, Fenoy S, Oyibo WA, Del Aguila C, et al. Genotypes of Cryptosporidium spp. and Enterocytozoon bieneusi in human immunodeficiency virus-infected patients in Lagos, Nigeria. J Eukaryot Microbiol. 2016;63(4):414–8.
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(2):e0003529.
Ad L, Amor-Aramendía A, Bailo B, Saugar JM, Anegagrie M, Arroyo A, et al. Prevalence and genetic diversity of Giardia duodenalis and Cryptosporidium spp. among school children in a rural area of the Amhara Region, North-West Ethiopia. PLoS One. 2016;11(7):e0159992.
Graczyk T, DaSilva A, Cranfield M, Nizeyi J, Kalema G, Pieniazek N. Cryptosporidium parvum genotype 2 infections in free-ranging mountain gorillas (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park, Uganda. Parasitol Res. 2001;87(5):368–70.
Abd El Kader NM, Blanco MA, Ali-Tammam M, Abd El Ghaffar Ael R, Osman A, El Sheikh N, et al. Detection of Cryptosporidium parvum and Cryptosporidium hominis in human patients in Cairo, Egypt. Parasitol Res. 2012;110(1):161–6.
Berrilli F, D’Alfonso R, Giangaspero A, Marangi M, Brandonisio O, Kaboré Y, et al. Giardia duodenalis genotypes and Cryptosporidium species in humans and domestic animals in Côte d’Ivoire: occurrence and evidence for environmental contamination. Trans R Soc Trop Med Hyg. 2012;106(3):191–5.
Salyer SJ, Gillespie TR, Rwego IB, Chapman CA, Goldberg TL. Epidemiology and molecular relationships of Cryptosporidium spp. in people, primates, and livestock from Western Uganda. PLoS Negl Trop Dis. 2012;6(4):e1597.
Ibrahim MA, Abdel-Ghany AE, Abdel-Latef GK, Abdel-Aziz SA, Aboelhadid SM. Epidemiology and public health significance of Cryptosporidium isolated from cattle, buffaloes, and humans in Egypt. Parasitol Res. 2016;115(6):2439–48.
Jiang J, Xiao L. An evaluation of molecular diagnostic tools for the detection and differentiation of human-pathogenic Cryptosporidium spp. J Eukaryot Microbiol. 2003;50 Suppl 1:542–7.
Amer S, Honma H, Ikarashi M, Tada C, Fukuda Y, Suyama Y, et al. Cryptosporidium genotypes and subtypes in dairy calves in Egypt. Vet Parasitol. 2010;169:382–6.
Amer S, Zidan S, Feng Y, Adamu H, Li N, Xiao L. Identity and public health potential of Cryptosporidium spp. in water buffalo calves in Egypt. Vet Parasitol. 2013;191:123–7.
Amer S, Zidan S, Adamu H, Ye J, Roellig D, Xiao L, et al. Prevalence and characterization of Cryptosporidium spp. in dairy cattle in Nile River delta provinces, Egypt. Exp Parasitol. 2013;135(3):518–23.
Mahfouz ME, Mira N, Amer S. Prevalence and genotyping of Cryptosporidium spp. in farm animals in Egypt. J Vet Med Sci. 2014;76(12):1569–75.
Rahmouni I, Essid R, Aoun K, Bouratbine A. Glycoprotein 60 diversity in Cryptosporidium parvum causing human and cattle cryptosporidiosis in the rural region of Northern Tunisia. Am J Trop Med Hyg. 2014;90(2):346–50.
Mbae C, Mulinge E, Waruru A, Ngugi B, Wainaina J, Kariuki S. Genetic diversity of Cryptosporidium in children in an urban informal settlement of Nairobi, Kenya. PLoS One. 2015;10(12):e0142055.
Geurden T, Goma FY, Siwila J, Phiri IGK, Mwanza AM, Gabriel S, et al. Prevalence and genotyping of Cryptosporidium in three cattle husbandry systems in Zambia. Vet Parasitol. 2006;138(3):217–22.
Goma FY, Geurden T, Siwila J, Phiri IGK, Gabriel S, Claerebout E, et al. The prevalence and molecular characterisation of Cryptosporidium spp. in small ruminants in Zambia. Small Rumin Res. 2007;72(1):77–80.
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(7):733–4.
Lalle M, Bruschi F, Castagna B, Campa M, Pozio E, Cacciò SM. High genetic polymorphism among Giardia duodenalis isolates from Sahrawi children. Trans R Soc Trop Med Hyg. 2009;103(8):834–8.
Johnston AR, Gillespie TR, Rwego IB, McLachlan TLT, Kent AD, Goldberg TL. Molecular epidemiology of cross-species Giardia duodenalis transmission in western Uganda. PLoS Negl Trop Dis. 2010;4(5):e683.
Soliman RH, Fuentes I, Rubio JM. Identification of a novel Assemblage B subgenotype and a zoonotic Assemblage C in human isolates of Giardia intestinalis in Egypt. Parasitol Int. 2011;60(4):507–11.
Sak B, Petrzelkova KJ, Kvetonova D, Mynarova A, Shutt KA, Pomajbikova K, et al. Long-term monitoring of Microsporidia, Cryptosporidium and Giardia 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(8):e71840.
Di Cristanziano V, Santoro M, Parisi F, Albonico M, Shaali MA, Di Cave D, et al. Genetic characterization of Giardia duodenalis by sequence analysis in humans and animals in Pemba Island, Tanzania. Parasitol Int. 2014;63(2):438–41.
Hogan JN, Miller WA, Cranfield MR, Ramer J, Hassell J, Noheri JB, et al. Giardia in mountain gorillas (Gorilla beringei beringei), forest buffalo (Syncerus caffer), and domestic cattle in Volcanoes National Park, Rwanda. J Wildl Dis. 2014;50(1):21–30.
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.
Jagai JS, Castronovo DA, Monchak J, Naumova EN. Seasonality of cryptosporidiosis: a meta-analysis approach. Environ Res. 2009;109(4):465–78.
Lal A, Hales S, French N, Baker MG. Seasonality in human zoonotic enteric diseases: a systematic review. PLoS One. 2012;7(4):e31883.
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(2):102–8.
Gatei W, Wamae CN, Mbae C, Waruru A, Mulinge E, Waithera T, et al. Cryptosporidiosis: prevalence, genotype analysis, and symptoms associated with infections in children in Kenya. Am J Trop Med Hyg. 2006;75(1):78–82.
Kange’the E, McDermott B, Grace D, Mbae C, Mulinge E, Monda J, et al. Prevalence of cryptosporidiosis in dairy cattle, cattle-keeping families, their non-cattle-keeping neighbours and HIV-positive individuals in Dagoretti Division, Nairobi, Kenya. Trop Anim Health Prod. 2012;44:11–6.
El-Badry AA, Al-Antably ASA, Hassan MA, Hanafy NA, Abu-Sarea EY. Molecular seasonal, age and gender distributions of Cryptosporidium in diarrhoeic Egyptians: distinct endemicity. Eur J Clin Microbiol Infect Dis. 2015;34(12):2447–53.
Ismail MA, El-Akkad DM, Rizk EM, El-Askary HM, El-Badry AA. Molecular seasonality of Giardia lamblia in a cohort of Egyptian children: a circannual pattern. Parasitol Res. 2016;115(11):4221–7.
Nazeer JT, El Sayed Khalifa K, von Thien H, El-Sibaei MM, Abdel-Hamid MY, Tawfik RA, et al. Use of multiplex real-time PCR for detection of common diarrhea causing protozoan parasites in Egypt. Parasitol Res. 2013;112(2):595–601.
Banisch DM, El-Badry A, Klinnert JV, Ignatius R, El-Dib N. Simultaneous detection of Entamoeba histolytica/dispar, Giardia duodenalis and cryptosporidia by immunochromatographic assay in stool samples from patients living in the Greater Cairo Region, Egypt. World J Microbiol Biotechnol. 2015;31(8):1251–8.
Krumkamp R, Sarpong N, Schwarz NG, Adelkofer J, Loag W, Eibach D, et al. Gastrointestinal infections and diarrheal disease in Ghanaian infants and children: an outpatient case-control study. PLoS Negl Trop Dis. 2015;9(3):e0003568.
Wasike WE, Kutima HL, Muya MS, Wamachi A. Epidemiology of Cryptosporidium spp. and other enteric parasites in children up to five years of age in Bungoma County, Kenya. J Biol Food Sci Res. 2015;4(1):1–6.
Wanyiri JW, Kanyi H, Maina S, Wang DE, Ngugi P, O’Connor R, et al. Infectious diarrhoea in antiretroviral therapy-naive HIV/AIDS patients in Kenya. Trans R Soc Trop Med Hyg. 2013;107(10):631–8.
Bhavnani D, Goldstick JE, Cevallos W, Trueba G, Eisenberg JNS. Synergistic effects between rotavirus and coinfecting pathogens on diarrheal disease: Evidence from a community-based study in northwestern Ecuador. Am J Epidemiol. 2012;176(5):387–95.
Gatei W, Ashford RW, Beeching NJ, Kamwati SK, Greensill J, Hart CA. Cryptosporidium muris infection in an HIV-infected adult, Kenya. Emerg Infect Dis. 2002;8(2):204–6.
Essid R, Mousli M, Aoun K, Abdelmalek R, Mellouli F, Kanoun F, et al. Identification of Cryptosporidium species infecting humans in Tunisia. Am J Trop Med Hyg. 2008;79(5):702–5.
Molloy SF, Smith HV, Kirwan P, Nichols RA, Asaolu SO, Connelly L, et al. Identification of a high diversity of Cryptosporidium species genotypes and subtypes in a pediatric population in Nigeria. Am J Trop Med Hyg. 2010;82(4):608–13.
Anim-Baidoo I, Narh C, Obiri D, Ewerenonu-Laryea C, Donkor ES, Adjei DN, et al. Cryptosporidial diarrhoea in children at a paediatric hospital in Accra, Ghana. Int J Trop Dis Health. 2015;10(3):1–13.
Xiao L, Fayer R. Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. Int J Parasitol. 2008;38(11):1239–55.
Nazemalhosseini-Mojarad E, Feng Y, Xiao L. The importance of subtype analysis of Cryptosporidium spp. in epidemiological investigations of human cryptosporidiosis in Iran and other Mideast countries. Gastroenterol Hepatol Bed Bench. 2012;5(2):67–70.
Ryan UNA, Fayer R, Xiao L. Cryptosporidium species in humans and animals: current understanding and research needs. Parasitology. 2014;141(13):1667–85.
Morgan U, Weber R, Xiao L, Sulaiman I, Thompson RC, Ndiritu W, et al. Molecular characterization of Cryptosporidium isolates obtained from human immunodeficiency virus-infected individuals living in Switzerland, Kenya, and the United States. J Clin Microbiol. 2000;38(3):1180–3.
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(4):1458–62.
Akiyoshi DE, Tumwine JK, Bakeera-Kitaka S, Tzipori S. Subtype analysis of Cryptosporidium isolates from children in Uganda. J Parasitol. 2006;92(5):1097–100.
Morse TD, Nichols RA, Grimason AM, Campbell BM, Tembo KC, Smith HV. Incidence of cryptosporidiosis species in paediatric patients in Malawi. Epidemiol Infect. 2007;135(8):1307–15.
Blanco MA, Iborra A, Vargas A, Nsie E, Mba L, Fuentes I. Molecular characterization of Cryptosporidium isolates from humans in Equatorial Guinea. Trans R Soc Trop Med Hyg. 2009;103(12):1282–4.
Abda IB, Essid R, Mellouli F, Aoun K, Bejaoui M, Bouratbine A. Cryptosporidium infection in patients with major histocompatibility complex class II deficiency syndrome in Tunisia: description of five cases. Arch Pediatr. 2011;18(9):939–44.
Blanco MA, Montoya A, Iborra A, Fuentes I. Identification of Cryptosporidium subtype isolates from HIV-seropositive patients in Equatorial Guinea. Trans R Soc Trop Med Hyg. 2014;108(9):594–6.
Wasike WE, Kutima HL, Muya MS, Wamachi A. Diagnostic procedures, epidemiology and genetic diversity of Cryptosporidium species in Bungoma County, Kenya. Int J Sci Res. 2015;4(3):1135–40.
Samra NA, Jori F, Cacciò SM, Frean J, Poonsamy B, Thompson PN. Cryptosporidium genotypes in children and calves living at the wildlife or livestock interface of the Kruger National Park, South Africa. Onderstepoort J Vet Res. 2016;83(1):1–7.
Peng MM, Matos O, Gatei W, Das P, Stantic-Pavlinic M, Bern C, et al. A comparison of Cryptosporidium subgenotypes from several geographic regions. J Eukaryot Microbiol. 2001;48 Suppl 1:28s–31s.
Eida AM, Eida MM, El-Desoky A. Pathological studies of different genotypes of human Cryptosporidium Egyptian isolates in experimentally mice. J Egypt Soc Parasitol. 2009;39(3):975.
Williams SB, Jiri G, Richard NG. Cloning and Sequence Analysis of a highly polymorphic Cryptosporidium parvum gene encoding a 60-kilodalton glycoprotein and characterization of Its 15- and 45-kilodalton zoite surface antigen products. Infect Immun. 2000;68(7):4117–34.
Dyachenko V, Kuhnert Y, Schmaeschke R, Etzold M, Pantchev N, Daugschies A. Occurrence and molecular characterization of Cryptosporidium spp. genotypes in European hedgehogs (Erinaceus europaeus L.) in Germany. Parasitology. 2010;137(2):205–16.
Krawczyk AI, van Leeuwen AD, Jacobs-Reitsma W, Wijnands LM, Bouw E, Jahfari S, et al. Presence of zoonotic agents in engorged ticks and hedgehog faeces from Erinaceus europaeus in (sub) urban areas. Parasit Vectors. 2015;8:210.
Sangster L, Blake DP, Robinson G, Hopkins TC, Sa RCC, Cunningham AA, et al. Detection and molecular characterisation of Cryptosporidium parvum in British European hedgehogs (Erinaceus europaeus). Vet Parasitol. 2016;217:39–44.
Stensvold CR, Elwin K, Winiecka-Krusnell J, Chalmers RM, Xiao L, Lebbad M. Development and application of a gp60-based typing assay for Cryptosporidium viatorum. J Clin Microbiol. 2015;53(6):1891–7.
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(3):520–2.
Graczyk TK, Bosco-Nizeyi J, Ssebide B, Thompson RCA, Read C, Cranfield MR. Anthropozoonotic genotype (Assemblage) A infections in habitats of free-ranging human-habituated gorillas, Uganda. J Parasitol. 2002;88(5):905–9.
Gelanew T, Lalle M, Hailu A, Pozio E, Cacciò SM. Molecular characterization of human isolates of Giardia duodenalis from Ethiopia. Acta Trop. 2007;102(2):92–9.
Helmy MMF, Abdel-Fattah HS, Rashed L. Real-time PCR/RFLP assay to detect Giardia intestinalis genotypes in human isolates with diarrhea in Egypt. J Parasitol. 2009;95(4):1000–4.
Maikai BV, Umoh JU, Lawal IA, Kudi AC, Ejembi CL, Xiao L. Molecular characterizations of Cryptosporidium, Giardia, and Enterocytozoon in humans in Kaduna State, Nigeria. Exp Parasitol. 2012;131(4):452–6.
Sadek GS, El-Settawy MA, Nasr SA. Genotypic characterization of Giardia duodenalis in children in Menoufiya and Sharkiya governorates, Egypt. Life Sci J. 2013;10(1):3006–15.
Foronda P, Bargues MD, Abreu-Acosta N, Periago MV, Valero MA, Valladares B, et al. Identification of genotypes of Giardia intestinalis of human isolates in Egypt. Parasitol Res. 2008;103(5):1177–81.
Abdel-Moein KA, Saeed H. The zoonotic potential of Giardia intestinalis Assemblage E in rural settings. Parasitol Res. 2016;115(8):3197–202.
Syakalima M, Noinyane M, Ramaili T, Motsei L, Nyirenda M. A coprological assessment of cryptosporidiosis and giardiosis in pigs of mafikeng villages, north west province of South Africa. Indian J Anim Res. 2015;49(1):132–5.
Ghoneim NH, Abdel-Moein KA, Saeed H. Fish as a possible reservoir for zoonotic Giardia duodenalis Assemblages. Parasitol Res. 2012;110(6):2193–6.
Abubakar BA, Maikai BV, Ajogi I, Otolorin GR. Prevalence of Giardia cysts in household dog faeces within Zaria Metropolis, Kaduna State, Nigeria and its public health significance. J Vet Adv. 2015;5(8):1053–7.
Olabanji GM, Maikai BV, Otolorin GR. Prevalence and risk factors associated with faecal shedding of Cryptosporidium oocysts in dogs in the Federal Capital Territory, Abuja, Nigeria. Vet Med Int. 2016;2016:1–6.
Soltane R, Guyot K, Dei-Cas E, Ayadi A. Cryptosporidium parvum (Eucoccidiorida: Cryptosporiidae) in calves: results of a longitudinal study in a dairy farm in Sfax, Tunisia. Parasite. 2007;14(4):309–12.
Sabry MA, Taher ES, Meabed EMH. Prevalence and genotyping of zoonotic Giardia from Fayoum Governorate, Egypt. Res J Parasitol. 2009;4(4):105–4.
Baroudi D, Khelef D, Hakem A, Abdelaziz A, Chen X, Lysen C, Roellig D, Xiao L. Molecular characterization of zoonotic pathogens Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in calves in Algeria. Vet Parasitol. 2017(8):66–9.
Szonyi B, Kang’ethe EK, Mbae CK, Kakundi EM, Kamwati SK, Mohammed HO. First report of Cryptosporidium deer-like genotype in Kenyan cattle. Vet Parasitol. 2008;153(1):172–5.
Soltane R, Guyot K, Dei-Cas E, Ayadi A. Prevalence of Cryptosporidium spp. (Eucoccidiorida: Cryptosporiidae) in seven species of farm animals in Tunisia. Parasite. 2007;14(4):335–8.
Amer SER. Genotypic and phylogenetic characterization of Giardia intestinalis from human and dairy cattle in Kafr El Sheikh Governorate, Egypt. J Egypt Soc Parasitol. 2013;43(1):133–46.
van Zijll Langhout M, Reed P, Fox M. Validation of multiple diagnostic techniques to detect Cryptosporidium sp. and Giardia sp. in free-ranging western lowland gorillas (Gorilla gorilla gorilla) and observations on the prevalence of these protozoan infections in two populations in Gabon. J Zoo Wildl Med. 2010;41(2):210–7.
Nizeyi JB, Mwebe R, Nanteza A, Cranfield MR, Kalema GR, Graczyk TK. Cryptosporidium sp. and Giardia sp. infections in mountain gorillas (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park, Uganda. J Parasitol. 1999;85(6):1084–8.
Sak B, Petrzelková KJ, Kvetonová D, Mynárová A, Pomajbíková K, Modrý D, et al. Diversity of Microsporidia, Cryptosporidium and Giardia in mountain gorillas (Gorilla beringei beringei) in Volcanoes National Park, Rwanda. PLoS One. 2014;9(11):e109751.
Samra NA, 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(1):155–9.
Hope K, Goldsmith ML, Graczyk T. Parasitic health of olive baboons in Bwindi Impenetrable National Park, Uganda. Vet Parasitol. 2004;122(2):165–70.
Rasambainarivo FT, Gillespie TR, Wright PC, Arsenault J, Villeneuve A, Lair S. Survey of Giardia and Cryptosporidium in lemurs from the Ranomafana National Park, Madagascar. J Wildl Dis. 2013;49(3):741–3.
Kleinertz S, Hermosilla C, Ziltener A, Kreicker S, Hirzmann J, Abdel-Ghaffar F, et al. Gastrointestinal parasites of free-living indo-pacific bottlenose dolphins (Tursiops aduncus) in the Northern Red Sea, Egypt. Parasitol Res. 2014;113(4):1405–15.
Li W, Kiulia NM, Mwenda JM, Nyachieo A, Taylor MB, Zhang X, et al. Cyclospora papionis, Cryptosporidium hominis, and human-pathogenic Enterocytozoon bieneusi in captive baboons in Kenya. J Clin Microbiol. 2011;49(12):4326–9.
Li N, Xiao L, Alderisio K, Elwin K, Cebelinski E, Chalmers R, et al. Subtyping Cryptosporidium ubiquitum, a zoonotic pathogen emerging in humans. Emerg Infect Dis. 2014;20(2):217–24.
Teichroeb JA, Kutz SJ, Parkar U, Thompson RC, Sicotte P. Ecology of the gastrointestinal parasites of Colobus vellerosus at Boabeng-Fiema, Ghana: possible anthropozoonotic transmission. Am J Phys Anthropol. 2009;140(3):498–507.
Futagbi G, Agyei DO, Aboagye IF, Yirenya-Tawiah DR, Edoh DA. Intestinal parasites of the grasscutter (Thryonomys swinderianus Temminck 1827) from the Kwaebibirem District of the Eastern Region of Ghana. West Afr J Appl Ecol. 2010;17:81–7.
Nizeyi JB, Sebunya D, Dasilva AJ, Cranfield MR, Pieniazek NJ, Graczyk TK. Cryptosporidiosis in people sharing habitats with free-ranging mountain gorillas (Gorilla gorilla beringei), Uganda. Am J Trop Med Hyg. 2002;66(4):442–4.
Smith HV, Forbes GI, Patterson WJ, Hardie R, Greene LA, Benton C, et al. An outbreak of waterborne cryptosporidiosis caused by post-treatment contamination. Epidemiol Infect. 1989;103(3):703–15.
Sorvillo FJ, Fujioka K, Nahlen B, Tormey MP, Kebabjian R, Mascola L. Swimming-associated cryptosporidiosis. Am J Public Health. 1992;82(5):742–4.
Mac Kenzie WR, Rose JB, Davis JP, Hoxie NJ, Proctor ME, Gradus MS, et al. A massive outbreak in milwaukee of Cryptosporidium infection transmitted through the public water supply. N Engl J Med. 1994;331(3):161–7.
Fayer R. Cryptosporidium: a water-borne zoonotic parasite. Vet Parasitol. 2004;126(1):37–56.
Smith A, Reacher M, Smerdon W, Adak GK, Nichols G, Chalmers RM. Outbreaks of waterborne infectious intestinal disease in England and Wales, 1992–2003. Epidemiol Infect. 2006;134(6):1141–9.
Robertson LJ, Forberg T, Hermansen L, Gjerde BK, Langeland N. Molecular characterisation of Giardia isolates from clinical infections following a waterborne outbreak. J Infect. 2007;55(1):79–88.
Daly ER, Roy SJ, Blaney DD, Manning JS, Hill VR, Xiao L, et al. Outbreak of giardiasis associated with a community drinking-water source. Epidemiol Infect. 2010;138(4):491–500.
Baldursson S, Karanis P. Waterborne transmission of protozoan parasites: Review of worldwide outbreaks - an update 2004–2010. Water Res. 2011;45(20):6603–14.
Budu-Amoako E, Greenwood SJ, Dixon BR, Barkema HW, McClure JT. Foodborne illness associated with Cryptosporidium and Giardia from livestock. J Food Prot. 2011;74(11):1944.
Karon AE, Hanni KD, Mohle-Boetani JC, Beretti RA, Hill VR, Arrowood M, et al. Giardiasis outbreak at a camp after installation of a slow-sand filtration water-treatment system. Epidemiol Infect. 2011;139(5):713–7.
Bedard BA, Elder R, Phillips L, Wachunas MF. Giardia outbreak associated with a roadside spring in Rensselaer County, New York. Epidemiol Infect. 2016;144(14):3013–6.
Abougrain AK, Nahaisi MH, Madi NS, Saied MM, Ghenghesh KS. Parasitological contamination in salad vegetables in Tripoli-Libya. Food Control. 2010;21(5):760–2.
El Said Said D. Detection of parasites in commonly consumed raw vegetables. Alex J Med. 2012;48(4):345–52.
Duedu KO, Yarnie EA, Tetteh-Quarcoo PB, Attah SK, Donkor ES, Ayeh-Kumi PF. A comparative survey of the prevalence of human parasites found in fresh vegetables sold in supermarkets and open-aired markets in Accra, Ghana. BMC Res Notes. 2014;7:836.
Tefera T, Biruksew A, Mekonnen Z, Eshetu T. Parasitic contamination of fruits and vegetables collected from selected local markets of Jimma town, southwest Ethiopia. Int Sch Res Not. 2014;2014:382715.
Mohamed MA, Siddig EE, Elaagip AH, Edris AMM, Nasr AA. Parasitic contamination of fresh vegetables sold at central markets in Khartoum state, Sudan. Ann Clin Microbiol Antimicrob. 2016;15:17.
Ayeh-Kumi PF, Tetteh-Quarcoo PB, Duedu KO, Obeng AS, Addo-Osafo K, Mortu S, et al. A survey of pathogens associated with Cyperus esculentus L. (tiger nuts) tubers sold in a Ghanaian city. BMC Res Notes. 2014;7:343.
Mladineo I, Trumbic Z, Jozic S, Šegvic T. First report of Cryptosporidium sp. (Coccidia, Apicomplexa) oocysts in the black mussel (Mytilus galloprovincialis) reared in the Mali Ston Bay, Adriatic Sea. J Shellfish Res. 2009;28(3):541–6.
Sutthikornchai C, Popruk S, Chumpolbanchorn K, Sukhumavasi W, Sukthana Y. Oyster is an effective transmission vehicle for Cryptosporidium infection in human. Asian Pac J Trop Med. 2016;9(6):562–6.
Hassan A, Farouk H, Hassanein F, Abdul-Ghani R. Currency as a potential environmental vehicle for transmitting parasites among food-related workers in Alexandria, Egypt. Trans R Soc Trop Med Hyg. 2011;105(9):519–24.
The International Network to Promote Household Water Treatment and Safe Storage. Combating waterborne disease at the household level. World Health Organization, Geneva. 2007. http://www.who.int/water_sanitation_health/publications/combating_diseasepart1lowres.pdf. Accessed 25 Sept 2016.
Centers for Disease Control and Prevention. Domestic Water, Sanitation, and Hygiene Epidemiology, Atlanta, USA.. 2015. http://www.cdc.gov/ncezid/dfwed/waterborne/global.html. Accessed 25 Sept 2016.
Tiwari SK, Jenkins MW. Point-of-use treatment options for improving household water quality among rural populations in the River Njoro watershed, Kenya. University of California- Davis, Global Livestock CRSP. 2008. http://crsps.net/resource/point-of-use-treatment-options-for-improving-household-water-quality-among-rural-populations-in-the-river-njoro-watershed-kenya/. Accessed 25 Sept 2016.
Yongsi HBN. Suffering for water, suffering from water: access to drinking-water and associated health risks in Cameroon. J Health Popul Nutr. 2010;28(5):424–35.
World Health Statistics. World Health Organisation, Geneva. 2014. http://apps.who.int/iris/bitstream/10665/112738/1/9789240692671_eng.pdf. Accessed 25 Sept 2016.
Munthali SM. Transfrontier conservation areas: Integrating biodiversity and poverty alleviation in Southern Africa. Nat Resour Forum. 2007;31:51–60.
Sente C, Erume J, Naigaga I, Mulindwa J, Ochwo S, Magambo PK, et al. Prevalence of pathogenic free-living Amoeba and other protozoa in natural and communal piped tap water from Queen Elizabeth protected area, Uganda. Infect Dis Poverty. 2016;5(1):68.
Kpoda NW, Oueda A, Somé YSC, Cissé G, Maïga AH, Kabré GB. Physicochemical and parasitological quality of vegetables irrigation water in Ouagadougou city, Burkina-Faso. Afr J Microbiol Res. 2015;9(5):307–17.
Ajeagah G, Njine T, Foto S, Bilong CB, Karanis P. Enumeration of Cryptosporidium sp. and Giardia sp. (oo)cysts in a tropical eutrophic lake. Int J Environ Sci Technol. 2007;4(2):223–32.
Ajeagah GA. Occurrence of bacteria, protozoans and metazoans in waters from two semi-urbanized areas of Cameroon. Ecohydrol Hydrobiol. 2013;13(3):218–25.
Yapo R, Koné B, Bonfoh B, Cissé G, Zinsstag J, Nguyen-Viet H. Quantitative microbial risk assessment related to urban wastewater and lagoon water reuse in Abidjan, Côte d’Ivoire. J Water Health. 2014;12(2):301–9.
Kwakye-Nuako G, Borketey P, Mensah-Attipoe I, Asmah R, Ayeh-Kumi P. Sachet drinking water in Accra: the potential threats of transmission of enteric pathogenic protozoan organisms. Ghana Med J. 2007;41(2):62–7.
Osei AS, Newman MJ, Mingle JAA, Ayeh-Kumi PE, Kwasi MO. Microbiological quality of packaged water sold in Accra, Ghana. Food Control. 2013;31(1):172–5.
Ndur S, Kuma J, Buah W, Galley J. Quality of Sachet water produced at Tarkwa, Ghana. Ghana Min J. 2016;15(1):22–34.
Youssef MY, Khalifa AM, el Azzouni MZ. Detection of cryptosporidia in different water sources in Alexandria by monoclonal antibody test and modified Ziehl Neelsen stain. J Egypt Soc Parasitol. 1998;28(2):487–96.
Ali MA, Al-Herrawy AZ, El-Hawaary SE. Detection of enteric viruses, Giardia and Cryptosporidium in two different types of drinking water treatment facilities. Water Res. 2004;38(18):3931–9.
Elshazly AM, Elsheikha HM, Soltan DM, Mohammad KA, Morsy TA. Protozoal pollution of surface water sources in Dakahlia Governorate, Egypt. J Egypt Soc Parasitol. 2007;37(1):51–64.
Abd El-Salam MM. Assessment of water quality of some swimming pools: a case study in Alexandria, Egypt. Environ Monit Assess. 2012;184(12):7395–406.
El-Kowrany SI, El-Zamarany EA, El-Nouby KA, El-Mehy DA, Ali EAA, Othman AA, et al. Water pollution in the Middle Nile Delta, Egypt: an environmental study. J Adv Res. 2016;7(5):781–94.
Fikrie N, Hailu A, Blete H. Determination and enumeration of Cryptosporidium oocysts and Giardia cysts in Legedadi (Addis Ababa) municipal drinking water system. Ethiop J Health Dev. 2008;22(1):68–70.
Atnafu T, Kassa H, Keil C, Fikrie N, Leta S, Keil I. Presence, Viability and determinants of Cryptosporidium oocysts and Giardia cysts in the Addis Ababa water supply and distribution system. Water Qual Expo Health. 2012;4(1):55–65.
Kato S, Ascolillo L, Egas J, Elson L, Gostyla K, Naples L, et al. Waterborne Cryptosporidium oocyst identification and genotyping: use of GIS for ecosystem studies in Kenya and Ecuador. J Eukaryot Microbiol. 2003;50 Suppl 1:548–9.
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(1):67–75.
Uneke CJ, Uneke BI. Occurrence of Cryptosporidium species in surface water in south-eastern Nigeria: the public health implication. Internet J Health. 2007;7(2):1–6.
Grundlingh M, De Wet CME. The search for Cryptosporidium oocysts and Giardia cysts in source water used for purification. Water SA. 2004;30(5):33–6.
Kfir R, Hilner C, Du Preez M, Bateman B. Studies on the prevalence of Giardia cysts and Cryptosporidium oocysts in South African water. Water Sci Technol. 1995;31(5-6):435–8.
Dungeni M, Momba MNB. The abundance of Cryptosporidium and Giardia spp. in treated effluents produced by four wastewater treatment plants in the Gauteng province of South Africa. Water SA. 2010;36(4):425–32.
Dobrowsky P, De Kwaadsteniet M, Cloete T, Khan W. Distribution of indigenous bacterial pathogens and potential pathogens associated with roof-harvested rainwater. Appl Environ Microbiol. 2014;80(7):2307–16.
Samie A, Ntekele P. Genotypic detection and evaluation of the removal efficiency of Giardia duodenalis at municipal wastewater treatment plants in northern South Africa. Trop Biomed. 2014;31(1):122–33.
Khouja LB, Cama V, Xiao L. Parasitic contamination in wastewater and sludge samples in Tunisia using three different detection techniques. Parasitol Res. 2010;107(1):109–16.
Ben Ayed L, Yang W, Widmer G, Cama V, Ortega Y, Xiao L. Survey and genetic characterization of wastewater in Tunisia for Cryptosporidium spp., Giardia duodenalis, Enterocytozoon bieneusi, Cyclospora cayetanensis and Eimeria spp. J Water Health. 2012;10(3):431–44.
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(4):1120–3.
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(3):435–7.
Dalu T, Barson M, Nhiwatiwa T. Impact of intestinal microorganisms and protozoan parasites on drinking water quality in Harare, Zimbabwe. J Water Sanit Hyg Dev. 2011;1(3):153–63.
Abubakar I, Aliyu SH, Arumugam C, Hunter PR, Usman NK. Prevention and treatment of cryptosporidiosis in immunocompromised patients. Cochrane Database Syst Rev. 2007;1:CD004932.
Amadi B, Mwiya M, Sianongo S, Payne L, Watuka A, Katubulushi M, et al. High dose prolonged treatment with nitazoxanide is not effective for cryptosporidiosis in HIV positive Zambian children: a randomised controlled trial. BMC Infect Dis. 2009;9:195.
The State of Food Insecurity in the World. Food and Agriculture Organisation. 2015. http://www.fao.org/3/a-i4646e.pdf. Accessed 23 September 2016.
Carr A, Marriott D, Field A, Vasak E, Cooper DA. Treatment of HIV-1-associated microsporidiosis and cryptosporidiosis with combination antiretroviral therapy. Lancet. 1998;351(9098):256–61.
Miao YM, Awad FM, Franzen C, Ellis DS, Müller A, Counihan HM, et al. Eradication of cryptosporidia and microsporidia following successful antiretroviral therapy. JAIDS J Acquir Immun Defic Syndr. 2000;25(2):124–9.
Gardner TB, Hill DR. Treatment of giardiasis. Clin Microbiol Rev. 2001;14(1):114–28.
Ansell BRE, McConville MJ, Ma’ayeh SY, Dagley MJ, Gasser RB, Svärd SG, et al. Drug resistance in Giardia duodenalis. Biotechnol Adv. 2015;33(6):888–901.
Solaymani-Mohammadi S, Genkinger JM, Loffredo CA, Singer SM. A meta-analysis of the effectiveness of albendazole compared with metronidazole as treatments for infections with Giardia duodenalis. PLoS Negl Trop Dis. 2010;4(5):e682.
Miyamoto Y, Eckmann L. Drug development against the major diarrhea-causing parasites of the small intestine, Cryptosporidium and Giardia. Front Microbiol. 2015;6(1208):1–17.
Rossignol J-F, Lopez-Chegne N, Julcamoro LM, Carrion ME, Bardin MC. Nitazoxanide for the empiric treatment of pediatric infectious diarrhea. Trans R Soc Trop Med Hyg. 2012;106(3):167–73.
Requena-Méndez A, Goñi P, Lóbez S, Oliveira I, Aldasoro E, Valls ME, et al. A family cluster of giardiasis with variable treatment responses: refractory giardiasis in a family after a trip to India. Clin Microbiol Infect. 2014;20(2):O135–O8.
Adams CP, Brantner VV. Estimating the cost of new drug development: is it really $802 million? Health Aff. 2006;25(2):420–8.
Chong CR, Sullivan DJ. New uses for old drugs. Nature. 2007;448(7154):645–6.
Bessoff K, Sateriale A, Lee KK, Huston CD. Drug repurposing screen reveals FDA-approved inhibitors of human HMG-CoA reductase and isoprenoid synthesis that block Cryptosporidium parvum growth. Antimicrob Agents Chemother. 2013;57(4):1804–14.
Debnath A, Ndao M, Reed SL. Reprofiled drug targets ancient protozoans: drug discovery for parasitic diarrheal diseases. Gut Microbes. 2013;4(1):66–71.
Bain LE, Awah PK, Geraldine N, Kindong NP, Siga Y, Bernard N, et al. Malnutrition in sub-Saharan Africa: burden, causes and prospects. Pan Afr Med J. 2013;15:120.
Boko M, Niang I, Nyong A, Vogel C, Githeko A, Medany O-EB, et al. Impacts, adaptation and vulnerability: contribution of working group II to the fourth assessment report of the intergovernmental panel on climate change. In: Parry ML, Canziani OF, Palutikof JP, Van der Linden PJ, Hanson CE, editors. Climate change. Cambridge: Cambridge University Press; 2007. p. 982.
Arnell NW. Climate change and global water resources: SRES emissions and socio-economic scenarios. Glob Environ Chang. 2004;14(1):31–52.
Ringler C, Zhu T, Cai X, Koo J. Climate change impacts on food security in sub-Saharan Africa: International Food Policy Research Institute, IFPRI Discussion Paper 01042. 2010. https://core.ac.uk/download/pdf/6237699.pdf. Accessed 23 Sept 2016.
Hofstra N, Vermeulen LC. Impacts of population growth, urbanisation and sanitation changes on global human Cryptosporidium emissions to surface water. Int J Hyg Environ Health. 2016;219(7):599–605.
Missaye A, Dagnew M, Alemu A, Alemu A. Prevalence of intestinal parasites and associated risk factors among HIV/AIDS patients with pre-ART and on-ART attending dessie hospital ART clinic, Northeast Ethiopia. AIDS Res Ther. 2013;10(1):7.
Kiros H, Nibret E, Munshea A, Kerisew B, Adal M. Prevalence of intestinal protozoan infections among individuals living with HIV/AIDS at Felegehiwot Referral Hospital, Bahir Dar, Ethiopia. Int J Infect Dis. 2015;35:80–6.
Mele R, Morales MAG, Tosini F, Pozio E. Indinavir reduces Cryptosporidium parvum infection in both in vitro and in vivo models. Int J Parasitol. 2003;33(7):757–64.
Global HIV Prevention: The access, funding, and leadership gaps. The Global HIV Prevention Working Group, Fact Sheet. 2009. http://www.issuelab.org/resource/global_hiv_prevention_the_access_funding_and_leadership_gaps. Accessed 25 Sept 2016.
The State of Food Insecurity in the World. Food and Agriculture Organisation. 2002. http://www.fao.org/docrep/005/y7352e/y7352e00.HTM. Accessed 25 Sept 2016.
Benouis A, Bekkouche Z, Benmansour Z. Epidemiological study of human intestinal parasitosis in the Hospital of Oran (Algeria). Int J Innov Appl Stud. 2013;2(4):613–20.
Hamaidi-Chergui F, Hamaidi MS, Benkhettar M, Mahieddine AO. Intestinal infections in Boufarik hospital (Blida) Algeria. Rev Ind Microbiol Sanit Environ. 2013;7(1):73–87.
Oliveira D, Ferreira FS, Atouguia J, Fortes F, Guerra A, Centeno-Lima S. Infection by intestinal parasites, stunting and anemia in school-aged children from Southern Angola. PLoS One. 2015;10(9):e0137327.
Gasparinho C, Mirante MC, Centeno-Lima S, Istrate C, Mayer AC, Tavira L, et al. Etiology of diarrhea in children younger than 5 years attending the Bengo General Hospital in Angola. Pediatr Infect Dis J. 2016;35(2):e28–34.
Sangaré I, Bamba S, Cissé M, Zida A, Bamogo R, Sirima C, et al. Prevalence of intestinal opportunistic parasites infections in the University Hospital of Bobo-Dioulasso, Burkina Faso. Infect Dis Poverty. 2015;4(1):1.
Richardson DJ, Callahan KD, Dondji B, Tsekeng P, Richardson KE. Prevalence of waterborne protozoan parasites in two rural villages in the West Province of Cameroon. Comp Parasitol. 2011;78(1):180–4.
Nkenfou CN, Nana CT, Payne VK. Intestinal parasitic infections in HIV infected and non-infected patients in a low HIV prevalence region, West-Cameroon. PLoS One. 2013;8(2):e57914.
Bissong M, Nguemain N, Ng’awono T, Kamga F. Burden of intestinal parasites amongst HIV/AIDS patients attending Bamenda Regional Hospital in Cameroon. Afr J Clin Exp Microbiol. 2015;16(3):97–103.
Ngum NH, Ngum AN, Jini SS. Opportunistic intestinal protozoan infections in HIV/AIDS patients on antiretroviral therapy in the North West Region of Cameroon. Br Microbiol Res J. 2015;7(6):269.
Bouyou-Akotet MK, Owono-Medang M, Moussavou-Boussougou MN, Mamfoumbi MM, Mintsa-Nguema R, Mawili-Mboumba DP, et al. Low sensitivity of the immunocardSTAT® Crypto/Giardia rapid assay test for the detection of Giardia and Cryptosporidium in fecal samples from children living in Libreville, Central Africa. J Parasit Dis. 2016;40(4):1179–83.
Hamit M, Tidjani M, Bilong CB. Recent data on the prevalence of intestinal parasites in N’Djamena, Chad Republic. Afr J Environ Sci Technol. 2008;2(12):407–11.
Korzeniewski K. Prevalence of intestinal protozoan infections among European UN peacekeepers in Chad, Central Africa. Int Rev Armed Forces Med Serv. 2012;85(2):57–61.
Becker SL, Chatigre JK, Gohou JP, Coulibaly JT, Leuppi R, Polman K, et al. Combined stool-based multiplex PCR and microscopy for enhanced pathogen detection in patients with persistent diarrhoea and asymptomatic controls from Côte d’Ivoire. Clin Microbiol Infect. 2015;21(6):591.
Berrilli F, Di Cave D, N’Guessan R, Kabore Y, Giangaspero A, Sorge RP, et al. Social determinants associated with Giardia duodenalis infection in southern Cote d’Ivoire. Eur J Clin Microbiol Infect Dis. 2014;33(10):1799–802.
Coulibaly JT, Ouattara M, D’Ambrosio MV, Fletcher DA, Keiser J, Utzinger J, et al. Accuracy of mobile phone and handheld light microscopy for the diagnosis of schistosomiasis and intestinal protozoa infections in Côte d’Ivoire. PLoS Negl Trop Dis. 2016;10(6):e0004768.
Wumba R, Longo-Mbenza B, Mandina M, Wobin TO, Biligui S, Sala J, et al. Intestinal parasites infections in hospitalized AIDS patients in Kinshasa, Democratic Republic of Congo. Parasite. 2010;17(4):321–8.
Mohammad KAE-A, Mohammad AAE-A. A survey of Giardia and Cryptosporidium spp. in rural and urban community in North Delta, Egypt. Zagazig Univ Med J. 2015;17(2):194–201.
Ibrahim RAS, Rabab Z, Gehan E-E, Mohamed E-M, Mohamed E-F, Eman A. Comparison between modified acid fast staining and antigen detection assay as diagnostic techniques for Cryptosporidium parvum. World J Med Sci. 2016;13(1):72–8.
El-Shabrawi M, Salem M, Abou-Zekri M, El-Naghi S, Hassanin F, El-Adly T, et al. The burden of different pathogens in acute diarrhoeal episodes among a cohort of Egyptian children less than five years old. Prz Gastroenterol. 2014;10(3):173–80.
Eraky MA, El-Hamshary AM, Hamadto HH, Abdallah KF, Abdel-Hafed WM, Abdel-Had S. Predominance of Cryptosporidium parvum genotype among diarrheic children from Egypt as an indicator for zoonotic transmission. Acta Parasitol. 2014;60(1):26–34.
Fathy MM, Abdelrazek NM, Hassan FA, El-Badry AA. Molecular copro-prevalence of Cryptosporidium in Egyptian children and evaluation of three diagnostic methods. Indian Pediatr. 2014;51(9):727–9.
Helmy YA, Krucken J, Nockler K, von Samson-Himmelstjerna G, Zessin KH. Comparison between two commercially available serological tests and polymerase chain reaction in the diagnosis of Cryptosporidium in animals and diarrhoeic children. Parasitol Res. 2014;113(1):211–6.
Shehata A, Hassanein F. Intestinal parasitic infections among mentally handicapped individuals in Alexandria, Egypt. Ann Parasitol Hum Comp. 2014;61(4):275–81.
Hassanein SM, Abd-El-Latif MM, Hassanin OM, Abd-El-Latif LM, Ramadan NI. Cryptosporidium gastroenteritis in Egyptian children with acute lymphoblastic leukemia: magnitude of the problem. Infection. 2012;40(3):279–84.
Roka M, Goni P, Rubio E, Clavel A. Prevalence of intestinal parasites in HIV-positive patients on the island of Bioko, Equatorial Guinea: its relation to sanitary conditions and socioeconomic factors. Sci Total Environ. 2012;432:404–11.
Roka M, Goñi P, Rubio E, Clavel A. Intestinal parasites in HIV-seropositive patients in the Continental Region of Equatorial Guinea: its relation with socio-demographic, health and immune systems factors. Trans R Soc Trop Med Hyg. 2013;107(8):502–10.
Getaneh A, Medhin G, Shimelis T. Cryptosporidium and Strongyloides stercoralis infections among people with and without HIV infection and efficiency of diagnostic methods for Strongyloides in Yirgalem Hospital, southern Ethiopia. BMC Res Notes. 2010;3:90.
Adamu H, Wegayehu T, Petros B. High Prevalence of diarrhoegenic intestinal parasite infections among non-ART HIV patients in Fitche Hospital, Ethiopia. PLoS One. 2013;8(8):e72634.