Open Access

Cryptosporidium and Giardia in Africa: current and future challenges

Parasites & Vectors201710:195

https://doi.org/10.1186/s13071-017-2111-y

Received: 11 October 2016

Accepted: 24 March 2017

Published: 20 April 2017

Abstract

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.

Keywords

Cryptosporidium Giardia Africa Molecular typing HIV Malnutrition Climate change

Background

Infectious diarrhoea is a major cause of death in children under 5 years old in Africa [1]. 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 [2].

The enteric protozoan parasites Cryptosporidium and Giardia are important causes of diarrhoeal disease [36], with Cryptosporidium the most common diarrhoea-causing protozoan parasite worldwide [7]. 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 [8]. It has been estimated that 2.9 million Cryptosporidium-attributable cases occur annually in children aged < 24 months in sub-Saharan Africa [9] and infection is associated with a greater than two-fold increase in mortality in children aged 12 to 23 months [8].

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 [5]. Most infections are self-limited but recurrences are common in endemic areas. Chronic infection can lead to weight loss and malabsorption [12] and is associated with stunting (low height for age), wasting (low weight for height) and cognitive impairment in children in developing countries [1315]. Furthermore, acute giardiasis may disable patients for extended periods and can elicit protracted post-infectious syndromes, including irritable bowel syndrome and chronic fatigue [16].

In Africa, GEMS reported that Giardia was not significantly positively associated with moderate-to-severe diarrhoea [8]. 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 [19].

In addition to diarrhoea, both protozoans have been associated with abdominal distension, vomiting, fever and weight loss in mostly children and HIV/AIDS individuals [2029]. Malnutrition, which impairs cellular immunity, is an important risk factor for cryptosporidiosis [30] and Cryptosporidium infection in children is associated with malnutrition, persistent growth retardation, impaired immune response and cognitive deficits [3133]. The mechanism by which Cryptosporidium affects child growth seems to be associated with inflammatory damage to the small intestine [34]. Undernutrition (particularly in children) is both a sequela of, and a risk factor for, cryptosporidiosis [33, 3540]. For both parasites, breast-feeding is associated with protection against clinical cryptosporidiosis and giardiasis [19, 4143], even though it does not generally prevent acquisition of Giardia infection or chronic carriage [19].

Currently 31 Cryptosporidium species are considered valid [4448]. 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 [53]. Several studies also suggest that flies may play an important role in the mechanical transmission of Cryptosporidium and Giardia including human infectious species [5464].

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 [66]. 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 [67]. 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).
Table 1

Prevalence of Cryptosporidium and Giardia in African countries (2010–2016)

Country

Study population

Age group

Percentage positive for Giardia

(No. positive/No. tested)

Percentage positive for Cryptosporidium (No. positive/No. tested)

Diagnostic technique

Genotyping

(target gene)

Reference

Algeria

Patients with digestive disorders

≤ 80 years

3.6% (38/1042)

0.1% (1/1042)

Direct wet mount, formal ether concentration, iodine solution and acid fast staining

Not genotyped

[271]

Algeria

Sporadic cases

≤ 75 years

41.7% (25/542)

Iodine staining

Not genotyped

[272]

Angola

Children (with and without diarrhoea)

≤ 12 years

0.1% (44/328); 21.6% (73/338)

30.0% (101/337)

Iodine and acid fast staining, and immunoassay

Not genotyped

[273, 274]

Botswana

Children with diarrhoea

< 5 years

 

60.0% (45/75)

Not stated

Not genotyped

[41]

Burkina Faso

Patients with diarrhoea

All ages

 

26.5% (77/291)

Acid fast staining

Not genotyped

[275]

Cameroon

Individuals from Nloh and Bawa villages

Not specified

7.1% (14/197)

1.5% (3/194)

Immunoassay

Not genotyped

[276]

Cameroon

HIV/AIDS-positive and negative individuals

15–70 years

0.3% (1/396)

2.5% (10/396); 6.0% (12/200); 14.4% (46/320)

Direct microscopy, formal ether concentration, iodine and acid fast staining

Not genotyped

[277279]

Central Africa Republic

Employees at Dzanga-Sangha Park

Not specified

2.1% (1/48)

 

PCR

tpi

[122]

Central African Republic

Children (with and without diarrhoea)

Not stated; < 5 years

15.6% (27/173); 4.4% (29/666)

10.4% (18/173); 7.7% (51/666)

Merthiolate iodine formaldehyde concentration, acid fast staining, immunoassay and multiplex PCR

Not genotyped

[29, 280]

Chad

Individuals from different regions

≤ 76 years

3.5% (16/462)

 

Merthiolate-iodine-formaldehyde concentration

Not genotyped

[281]

Chad

European military UN peace keepers

21–51 years

22.3% (55/247)

 

Direct microscopy and iodine staining

Not genotyped

[282]

Côte d’Ivoire

Individuals with intestinal disorders, persistent diarrhoea and controls

≥ 1 year

19.9% (61/307); 29.0% (39/136)

6.2% (19/307); 8.8% (12/136)

Direct microscopy, iodine staining, formol ethyl-acetate concentration, formalin-ether concentration, immunoassay and PCR

bg; 18S rRNA; COWP

[106, 283]

Côte d’Ivoire

Children

≤ 19 years

21.6% (66/306); 20.7% (25/121)

 

Direct microscopy, iodine staining, formol-ethyl acetate concentration, ether-concentration technique

Not genotyped

[284, 285]

Democratic Republic of Congo

HIV/AIDS-positive individuals

15–73 years

1.7% (3/175)

9.7% (17/175); 5.4% (13/242)

Modified Ritchie formalin-ether concentration, acid fast staining and PCR assay

18S rRNA

[28, 286]

Egypt

Individuals with livestock in their household

≤ 60 years

 

19.0% (55/290)

Acid fast staining

COWP

[108]

Egypt

Individuals with and without diarrhoea

All ages

12.5% (15/150) to 27.3% (75/330)

5.9% (23/391) to 72.2% (52/92

Direct microscopy, formalin-ethyl acetate sedimentation, acid fast, iodine and trichrome staining, immunoassay and PCR

COWP; tpi; gdh; bg

[105, 121, 131, 287, 288]

Egypt

Children (with and without diarrhoea)

< 18 years

18.9% (224/1187) to 29.2% (47/161)

2.1% (15/707) to 49.1% (81/165)

Direct microscopy, modified Ritchie’s biphasic concentration, iodine and acid fast staining, immunoassay and PCR

18S rRNA; TRAP-C2; COWP; tpi; gdh; bg

[26, 80, 95, 132, 167, 289292]

Egypt

Mentally handicapped individuals

All ages

8.5% (17/200)

23.5% (47/200)

Trichrome and acid fast staining

Not genotyped

[293]

Egypt

Children with acute lymphoblastic leukemia and controls

≤ 15 years

 

18.2% (10/55)

Acid fast staining and serum immunoassay

Not genotyped

[294]

Egypt

Municipality solid-waste workers

21–59 years

3.8% (13/346)

23.4% (81/346)

Formol-ether concentration and acid fast staining

Not genotyped

[67]

Equatorial Guinea

HIV-positive and negative individuals

≤ 76 years

14.2% (44/310); 4.2% (14/333)

2.7% (9/333) to 18.1% (31/171)

Direct microscopy, formol-ether concentration, iodine and acid fast staining, Immunoassay and PCR

COWP

[152, 295, 296]

Ethiopia

HIV-positive and negative individuals

≤ 86 years

4.0% (15/378) to 7.9% (39/491)

8.5% (32/378) to 26.9% (140/520)

Direct microscopy, formol-ether concentration, iodine and acid fast staining and PCR

18S rRNA

[23, 267, 297300]

Ethiopia

Children

≤ 15 years

4.6% (16/350) to 55.0% (216/393)

4.6% (18/393) to 7.3% (28/348)

Direct microscopy, formol-ether concentration, iodine and acid fast staining, immunoassay and PCR

18S rRNA; tpi; gdh; bg

[103, 125, 299, 301]

Ethiopia

Individuals with diarrhoea or gastrointestinal symptoms

≤ 80 years

10.9% (10/92)

1.1% (1/92); 7.6% (79/1034)

Direct microscopy, acid fast staining, immunoassay and PCR

18S rRNA; COWP; gdh; bg

[82, 99]

Ghana

Children (with and without diarrhoea/gastrointestinal symptoms)

≤ 17 years

1.0% (1/101) to 37.9% (455/1199)

4.9% (59/1199) to 8.5% (204/2400)

Direct microscopy, formol-ether concentration, iodine and acid fast staining, immunoassay and PCR

18S rRNA; gdh

[98, 135, 302305]

Ghana

HIV-positive and negative individuals

All ages

12.6% (101/800)

8.2% (34/413); 9.0% (72/800)

Direct microscopy, formol-ether concentration, iodine and acid fast staining

Not genotyped

[306, 307]

Ghana

Food vendors

10–70 years

10.7% (15/140)

 

Direct microscopy, iodine staining and formalin-ether concentration

Not genotyped

[308]

Guinea-Bissau

Children from villages

≤ 7.5 years

56.0% (28/50)

 

Ritchie concentration method and PCR

18S rRNA; bg

[309]

Guinea Bissau

Children (with and without malnutrition)

< 5 years

33.9% (37/109)

 

Direct microscopy

Not genotyped

[310]

Kenya

Certified food-handlers

≥ 18 years

1.3% (4/312)

 

Iodine staining

Not genotyped

[311]

Kenya

HIV/AIDS-positive patients

≥ 18 years

 

34.1% (56/164)

Immunoassay and PCR

18S rRNA

[25]

Kenya

Individuals in villages

≤ 81 years

41.3% (329/796)

<1%

Multi-parallel qPCR

Not genotyped

[81]

Kenya

Children (with and without diarrhoea)

≤ 15 years

4.6% (98/2112) to 11.1% (109/981)

3.7% (36/981) to 9.8% (31/317)

Direct microscopy, formal-ether concentration, acid fast staining, immunoassay and PCR

18S rRNA; tpi; gdh; bg

[71, 88, 115, 136, 312, 313]

Libya

Children with diarrhoea

≤ 5 years

1.3% (3/239)

2.1% (5/239)

Immunoassays

Not genotyped

[314]

Libya

Individuals with diarrhoea

Not specified

1.3% (4/305)

2.3% (7/305)

Direct microscopy, iodine, eosin and acid fast staining, concentration methods

Not genotyped

[315]

Madagascar

Children (with and without diarrhoea)

< 5 years

11.7% (314/2692)

 

Direct microscopy and iodine staining

Not genotyped

[316]

Madagascar

Individuals from rural southeastern Madagascar

Not specified

 

0.8% (1/120)

PCR-RFLP

18S rRNA

[97]

Mali

European soldiers

Not specified

3.8% (2/53)

5.7% (3/53)

Multiplex real time PCR

Not genotyped

[317]

Morocco

Children (urban and rural)

5–15 years

12.5% (84/673)

 

Iodine, acid fast and Giemsa staining and Faust’s and Ritchie’s concentration methods

18S rRNA; gdh

[318]

Mozambique

HIV-positive and negative individuals

< 5 years

6.5% (6/93)

 

Direct microscopy and Ritchie’s concentration method

Not genotyped

[319]

Nigeria

Children (with and without diarrhoea or gastroenteritis)

≤ 15 years

37.2% (74/199)

1.0% (2/199) to 46.8% (88/188)

Direct microscopy, acid fast staining, immunoassay and qPCR (18S rRNA gene)

18S rRNA

[86, 87, 141, 320323]

Nigeria

HIV/AIDS-positive and negative individuals

≤ 80 years

1.9% (9/476) to 3.2% (5/157)

1.9% (3/157) to 35.9% (171/476)

Direct microscopy, acid fast staining, PCR-RFLP

18S rRNA; tpi; ITS rDNA

[83, 101, 166, 324, 325]

Rwanda

Children

≤ 18 years

35.7% (222/622); 59.7% (366/583)

 

Direct microscopy, ether-based concentration, real-time

PCR assays and multiplex qPCR

tpi

[22, 24, 326]

São Tomé and Príncipe

Children (with and without diarrhoea)

≤ 10 years

8.3% (29/348); 41.7% (185/444)

5.5% (19/348)

Direct microscopy, modified water-ether sedimentation, formol-ether concentration, iodine and acid fast staining and PCR-RFLP

18S rRNA; tpi

[96, 327]

Senegal

Children (with and without diarrhoea)

< 15 years

 

6.13% (23/375)

Acid fast stain and immunoassay

Not genotyped

[328]

South Africa

Children (with and without diarrhoea)

≤ 11 years

9.9% (16/162)

5.6% (8/143); 12.2% (54/442)

Acid fast staining and PCR

18S rRNA

[89, 154, 329]

South Africa

HIV-positive individuals

All ages

11.9% (18/151)

65.5% (165/252); 26.5% (40/151)

Acid fast stain, immunoassay, qPCR, PCR (18S rDNA) and loop-mediated isothermal amplification (LAMP)

Not genotyped

[330, 331]

Sudan

Inhabitants of rural areas

All ages

 

13.3% (115/866)

Acid fast staining

Not genotyped

[332]

Sudan

Children (with and without diarrhoea)

≤ 13 years and primary school-aged

10.1% (91/900) to 33.4% (167/500)

 

Direct microscopy and concentration technique

Not genotyped

[333336]

Sudan

Food handlers

4–57 years

20.5% (16/259)

 

Direct microscopy

Not genotyped

[337]

Sudan

Individuals with diarrhoea

1–80 years

22.0% (22/100)

 

Direct microscopy, formal ether concentration technique

Not genotyped

[338]

Tanzania

Individuals with and without diarrhoea

All ages

6.9% (218/3152); 53.4% (93/174)

1.1% (2/174)

Formol-ether-concentration technique, iodine and acid fast staining, qPCR and conventional PCR

18S rRNA

[339, 340]

Tanzania

Children (with and without diarrhoea)

< 5 years, school going age

1.9% (5/270) to 62.2% (28/45)

10.4% (131/1259); 18.9% (51/270)

Multiplex real-time PCR and immunoassays

18S rRNA; gdh

[72, 123, 341]

Tanzania

Individuals living in and around Gombe National Park

Not stated

 

4.3% (8/185)

PCR-RFLP

18S rRNA

[102]

Tanzania

HIV-positive individuals

30–43 years

9.6% (8/83)

 

Direct microscopy and iodine staining

Not genotyped

[342]

Tunisia

Children (with and without diarrhoea)

< 5 years

 

1.7% (7/403)

Acid fast staining

18S rRNA

[114]

Uganda

Individuals from villages near Kibale National

≤ 75 years

40.7% (44/108)

32.4% (35/108)

Real-time PCR, nested PCR

COWP; ef1-α; gdh; 18S rRNA; tpi

[107, 120]

Uganda

HIV-positive patients with Diarrhoea

10–69 years

 

3.6% (4/111)

Acid fast staining

Not genotyped

[343]

Uganda

Children (non-symptomatic and HIV seronegative)

≤ 12 years

20.1% (86/427)

12.5% (116/926)

Direct microscopy, acid fast staining and PCR

18S rRNA; bg; gdh; tpi

[344, 345]

Zambia

Pre-school children

≤ 7 years

29.0% (117/403) to 29.0% (228/786)

28.0% (113/403) to 30.7% (241/786)

Immunofluorescence stain

Not genotyped

[128, 346, 347]

Zimbabwe

Individuals in urban areas

All ages

2.7% (8/300)

6.3% (19/300)

Acid fast staining

Not genotyped

[348]

Abbreviations: bg, beta-giardin; COWP, Cryptosporidium oocyst wall protein gene; ef1-α, elongation factor 1-alpha; gdh, glutamate dehydrogenase; ITS, internal transcribed spacer; 18S rRNA, 18S ribosomal ribonucleic acid; tpi, triose phosphate isomerase gene; TRAP, thrombospondin-related adhesive protein

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 [69]. HIV status is an important host risk factor particularly for cryptosporidiosis and although Cryptosporidium is an important pathogen regardless of HIV-prevalence [8], HIV-positive children are between three and eighteen times more likely to have Cryptosporidium than those who are HIV-negative [7072]. The unfolding HIV/AIDS epidemic in African countries, with > 25 million adults and children infected with HIV/AIDS in 2015 [2], 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 [73] and malnutrition is an important risk factor for both diarrhoea and prolonged diarrhoea caused by Cryptosporidium and Giardia [19], 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, 7681]. 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, 82103] (Table 1), although some studies have relied on the Cryptosporidium oocyst wall protein (COWP) gene [26, 82, 92, 100, 104108], which is not as reliable as the 18S locus at identifying and differentiating Cryptosporidium species [109]. Subtyping of Cryptosporidium has been conducted mainly at the glycoprotein 60 (gp60) gene locus [23, 26, 82, 9395, 98, 100, 102, 108, 110115] (Table 2) while others targeted the heat shock protein 70 (HSP70) gene [91, 92, 100, 116118]. 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, 119124] (see Tables 1, 3 and 4).
Table 2

Cryptosporidium species and subtypes reported in humans from Africa

Country

Patient group

Cryptosporidium species (Prevalence in %)a

gp60 subtypes

Reference

Botswana

Children with diarrhoea (< 5 years)

C. parvum (50.0)

 

[41]

  

C. hominis (41.0)

  

Côte d’Ivoire

Individuals with intestinal disorders

C. meleagridis (75.0)

 

[106]

  

C. parvum (16.7)

  
  

C. hominis (8.3)

  

Democratic Republic of Congo

HIV-infected adults

C. hominis (80.0)

 

[28]

  

C. parvum (20.0)

  

Egypt

Individuals with livestock in their household

C. hominis (75.0)

 

[108]

  

C. parvum (25.0)

IIdA20G1

 

Egypt

Children with diarrhoea (≤ 10 years)

C. hominis (60.5)

 

[26]

  

C. parvum (38.3)

  

Egypt

Diarrhoeal patients

C. hominis (97.0)

 

[131]

  

C. parvum (3.0)

  

Egypt

Children with diarrhoea (1–14 years)

C. parvum (82.0)

 

[290]

  

C. hominis (12.0)

  
  

Mixed infections (6.0)

  

Egypt

Children with diarrhoea (< 10 years)

C. hominis (60.5)

 

[95]

  

C. parvum (38.3)

IIaA15G1R1; IIaA15G2R1; IIdA20G1a

 
  

C. parvum + C. bovis (1.2)

  

Egypt

Diarrhoeal patients

C. hominis (60.0)

 

[105]

  

C. parvum (20.0)

  
  

C. hominis + C. parvum (20.0)

  

Egypt

Gastrointestinal symptomatic patients

C. parvum (66.7)

 

[156]

  

C. hominis (27.7)

  
  

C. meleagridis (5.6)

  

Egypt

Immunocompromised patients

C. parvum (68.4)

 

[349]

  

C. hominis (26.3)

  
  

C. parvum + C. hominis (5.3)

  

Equatorial Guinea

HIV-infected and immunocompetent patients

C. parvum (52.9)

 

[150]

  

C. hominis (44.1)

  
  

C. meleagridis (2.9)

  

Equatorial Guinea

HIV-seropositive patients

C. parvum (54.8)

IIcA5G3b; IIeA10G1

[152]

  

C. hominis (50.0)

IaA18R3b; IaA24R3; IbA13G3; IdA15; IdA18b

 
  

C. meleagridis (3.2)

  

Ethiopia

Diarrhoeal patients (14–71 years)

C. parvum (95.1)

IIaA15G2R1b; IIaA16G2R1; IIaA16G1R1

[82]

  

C. hominis (2.4)

IbA9G3

 
  

C. hominis + C. parvum (2.4)

  

Ethiopia

HIV/AIDS patients

C. parvum (65.7)

IIaA13G2R1; IIaA14G2R1; IIaA15G2R1b; IIaA16G2R1; IIaA16G3R1; IIaA17G2R1; IIaA18G2R1; IIaA19G1R; IIbA12; IIcA5G3a; IIdA17G1; IIdA19G1; IIdA22G1; IIdA24G1; IIeA12G1; If-like

[23]

  

C. hominis (17.9)

IbA10G2; IdA20b; IdA24; IdA26; IeA11G3T3

 
  

C. viatorum (7.1)

  
  

C. felis (3.6)

  
  

C. meleagridis (2.1)

  
  

C. canis (1.4)

  
  

C. xiaoi (1.4)

  
  

C. hominis + C. parvum (0.7)

  

Ethiopia

Patients

C. hominis (100)

IbA9G3

[99]

Ethiopia

Cryptosporidium-positive (7 months to 27 years)

C. viatorum (90.0)

XVaA3d

[161]

Ethiopia

Children (6–15 years)

C. hominis (40.0)

 

[103]

  

C. viatorum (40.0)

  
  

C. parvum (20.0)

  

Ghana

Children (≤ 5 years)

C. parvum (100)

 

[142]

Ghana

Children with and without gastrointestinal symptoms

C. hominis (58.0)

IaA15T1R3; IaA15G1R4; IaA17; IaA18R3; IaA19R3; IaA21R3; IaA22R3; IaA24R3; IbA13G3b; IdA15; IeA11G3T3

[98]

  

C. parvum (42.1)

IIcA5G3ab; IIcA5G3b; IIeA10G1; IIeA10G2

 

Kenya

HIV patients

C. hominis (66.7)

 

[146]

  

C. parvum (16.7)

  
  

C. meleagridis (16.7)

  

Kenya

Not stated

C. hominis (C. parvum human) (90.0)

Ib; Ieb

[155]

  

C. meleagridis (10.0)

  

Kenya

An HIV-infected adult with diarrhoea

C. muris “rock hyrax”

 

[139]

Kenya

HIV-positive and negative children and adults

C. parvum human (69.7)

 

[147]

  

C. parvum bovine (21.2)

  
  

C. meleagridis (3.0)

  
  

C. muris (3.0)

  

Kenya

Children (< 5 years)

C. hominis (87.4)

 

[129]

  

C. parvum (8.6)

  
  

C. canis (1.7)

  
  

C. felis (1.1)

  
  

C. muris (0.6)

  
  

C. meleagridis (0.6)

  

Kenya

Children (≤ 5 years)

C. hominis (82.1)

 

[88]

  

C. parvum (17.9)

  

Kenya

HIV/AIDS patients with and without diarrhoea (≥ 18 years)

C. hominis (60.7)

Ia; Ibb; Id; Ie; If

[25]

  

C. parvum (23.2)

IIab; IIb; IIeb; IIc

 
  

C. canis (7.1)

  
  

C. meleagridis (5.3)

  
  

C. suis (3.6)

  

Kenya

HIV infected and uninfected children (5 years)

C. hominis (82.8)

IaA25R5; IaA27R3; IaA30R3; IaA7R1; IbA9G3; IbA9G3R2; IdA22; IdA24; IdA19; IdA25; IdA21; IdA20; IdA17G1; IdA18; IdA15G1; IdA23G1; IeA11G3T3R1b; IeA11G3T3; IfA19G1; IfA14G1; IfA12G1

[115]

  

C. parvum (11.9)

IIcA5G3R2

 
  

C. felis (2.6)

  
  

C. meleagridis (1.3)

  
  

C. parvum + C. hominis (0.7)

  

Kenya

Cryptosporidium spp.-positive female (25 years)

C. viatorum

XVaA3d

[161]

Kenya

Children (≤ 5 years)

C. hominis (38.9)

 

[153]

  

C. parvum (36.1)

  
  

C. meleagridis (16.7)

  
  

C. canis (5.6)

  
  

Unknown genotype (2.8)

  

Madagascar

Children with acute diarrhoeal disease (≤ 16 years)

C. hominis (91.7)

IaA22R3; IdA15G1b; IeA11G3T3

[350]

  

C. parvum (8.3)

IIcA5G3

 

Madagascar

Humans from rural south-eastern Madagascar

C. suis (100)

 

[97]

Malawi

HIV-positive and negative children

C. hominis (63.6)

 

[147]

  

C. parvum (36.4)

  

Malawi

Children HIV-positive and seronegative (≤ 30 months)

C. hominis (95.3)

Ia; Ib; Idb; Ie

[351]

  

C. parvum (4.7)

IIc; IIe

 

Malawi

Diarrhoeal children (< 5 years)

C. hominis (58.1)

 

[149]

  

C. parvum (23.3)

  
  

C. parvum + C. hominis (2.3)

  
  

C. parvum/C. hominis (9.3)

  
  

C. meleagridis (4.7)

  
  

C. muris/C. andersoni (2.3)

  

Nigeria

HIV-infected (majority) and non-infected patients

C. hominis (47.2)

IaA14R3; IaA16R3; IaA24R3; IaA25R3; IbA13G3; IeA11T3G3b

[83]

  

C. parvum (44.4)

IIcA5G3a; IIcA5G3h; New subtype family 1b; New subtype family 2

 
  

C. felis (5.6)

  
  

C. canis (2.8)

  

Nigeria

Children (6 months to 6 years)

C. hominis (44.2)

IaA18R2; IaA22R2; IaA24R2; IaA25R2; IaA28R2; IaA21R1; IbA10G2; IbA13G3b; IdA11; IdA17; IeA11G3T3b; Ih (Novel subtype); IhA14G1

[141]

  

C. parvum (32.5)

IIaA15G2R1; IIaA16G1R1; IIcA5G3ab; IIcA5G3b; IIiA11; IImA14G1

 
  

C. parvum plus C. hominis (5.2)

  
  

C. meleagridis (6.5)

  
  

C. cuniculus (C. rabbit genotype) (6.5)

  
  

C. ubiquitum (C. cervine genotype) (3.9)

  
  

C. canis (1.3)

  

Nigeria

Children (19.5–72 months)

C. hominis (37.3)

 

[86]

  

C. parvum (35.3)

  
  

C. parvum + C. hominis (7.8)

  
  

C. meleagridis (7.8)

  
  

C. cuniculus (C. rabbit genotype) (3.9)

  
  

C. ubiquitum (C. cervine genotype) (2.0)

  
  

C. canis (2.0)

  

Nigeria

Diarrhoeal and non-diarrhoeal children (1 to > 12 months)

C. hominis (60.0)

IaA24R3b; IbA13G3

[87]

  

C. parvum (40.0)

IIcA5G3k

 

Nigeria

Patients (2 months to 70 years)

C. hominis (66.7)

IaA23R3; IaA25R3

[166]

  

C. parvum (33.3)

IIeA10G1

 

Nigeria

HIV-infected patients (22–65 years)

C. hominis (50.0)

IeA11G3T3

[101]

  

C. parvum (25.0)

IIcA5G3k

 
  

C. meleagridis + C. hominis (25.0)

  

São Tomé and Príncipe

Children (2 months to 10 years)

C. hominis (73.7)

IeA11G3T3R1; IeA11G3T3; IaA27R3b; IaA23R3

[96]

  

C. parvum (26.3)

IIdA21G1a; IIdA26G1b; IIaA16G2R1; IIaA15G2R1

 

South Africa

Children (< 5 years)

C. hominis (75.0)

IbA12G3R2; IbA10G2; IeA11G3T3

[154]

  

C. meleagridis (25.0)

  

South Africa

Children (< 5 years)

C. hominis (76.0)

IaA20R3; IaA25G1R3; IaA17R3; IbA9G3; IbA10G1; IdA20; IdA25IdA26; IdA24; IeA11G3T3b; IfA14G1; IfA12G1

[89]

  

C. parvum (20.0)

IIbA11; IIcA5G3bb; IIeA12G1

 
  

C. meleagridis (4.0)

IIIdA4

 

South Africa

School children and hospital patients (≤ 88 years)

C. hominis (81.8)

 

[77]

  

C. parvum (18.2)

  

South Africa

HIV-infected children

C. hominis (75.0)

Ia; Ib; Id; Ie

[352]

  

C. parvum (25.0)

IIc

 

Tanzania

People living in and around Gombe National Park

C. hominis (100)

IfA12G2

[102]

Tanzania

Diarrhoeal children and controls (< 2 years old)

C. hominis (84.7)

 

[72]

  

C. parvum (7.6)

  
  

C. parvum or C. hominis (7.6)

  

Tanzania

HIV patients (18–65 years)

C. hominis (71.4)

 

[162]

  

C. parvum (28.6)

  

Tunisia

Children (< 5 years old)

C. parvum (57.1)

IIaA15G2R1b; IIdA16G1

[114]

  

C. meleagridis (42.9)

  

Tunisia

Children with primary immune deficiencies

C. hominis (40.0)

 

[151]

  

C. parvum (20.0)

  
  

C. meleagridis (20.0)

  
  

C. hominis/C. meleagridis (20.0)

  

Tunisia

Immunocompetent and immunodeficiency children

C. parvum (42.1)

 

[140]

  

C. hominis (36.8)

  
  

C. meleagridis (21.1)

  

Uganda

Volunteers (1.9 months to 75 years)

C. parvum (97.1)

 

[107]

  

C. parvum or C. hominis or C. cuniculus (2.9)

  

Uganda

Children (2–84 months)

C. hominis (74.4)

Ia; Ib; Id; Ieb

[148]

  

C. parvum (18.3)

IIcb; IIg; IIh; Iii

 
  

C. hominis + C. parvum (3.7)

  
  

C. meleagridis (3.7)

  

Uganda

Children with persistent diarrhoea, with and without HIV/AIDS (< 6 months)

C. hominis (73.7)

 

[70]

  

C. parvum (18.4)

  
  

C. parvum + C. hominis (3.9)

  
  

C. meleagridis (3.9)

  

Uganda

People who share habitats with free-ranging gorillas

C. parvum (100)

 

[191]

Zambia

Dairy farm workers and their household members

C. parvum (80.0)

 

[118]

  

C. hominis (20.0)

  

aPrevalence (percentage of species identified out of the total number of species genotyped per animal)

bDominant gp60 subtype

Table 3

Giardia duodenalis assemblages and subtypes reported in humans from Africa

Country

Patient group

Assemblage

(Prevalence in %)a

Subtype

Reference

Algeria

Children (8 and 13 years)

A (37.5)

AI; AIIb; Novel subtype

[119]

  

B (56.3)

BIII; BIV; Novel subtypes

 
  

A + B (6.3)

  

Central African Republic

Dzanga-Sangha Protected Areas Park employees

A (100)

AII

[122]

Côte d’Ivoire

Patients with intestinal disorders (2–63 years)

A (19.6)

 

[106]

  

B (76.8)

  
  

A + B (3.6)

  

Côte d’Ivoire

Patients with intestinal disorders (2–63 years)

A (34.4)

 

[106]

  

B (59.0)

  
  

A + B (6.6)

  

Egypt

Diarrhoeal patients (2–70 years)

A (6.7)

AI/AII

[121]

  

B (80.0)

BIII; B/BIII; BIV; BIII/BIVb

 
  

A + B (6.7)

  
  

C (6.7)

  

Egypt

Diarrhoeal patients (All ages)

A (18.8)

 

[132]

  

B (81.2)

  

Egypt

Children (< 10 years)

A (30.4)

AII

[80]

  

B (52.2)

  
  

E (8.7)

  
  

A/B (4.3)

  
  

A/E (4.3)

  

Egypt

Children (5–12 years)

A (77.1)

AII

[167]

  

B (22.9)

BIII

 

Egypt

Children with and without diarrhoea (1.5–12 years)

E (100)

 

[169]

Egypt

Diarrhoeal patients (4–65 years)

A (75.6)

AIb; AII

[165]

  

B (19.5)

  
  

A + B (5.0)

  

Egypt

Humans

A (5.0)

 

[168]

  

B (80.0)

  
  

E (15.0)

  

Ethiopia

Children (6–15 years)

A (17.9)

AIIb; AII/AIII

[103]

  

B (82.1)

BIII; BIVb; BIII/BIV

 

Ethiopia

Children (≤ 14 years)

A (22.9)

AIIb

[301]

  

B (77.1)

BIV; Novel subtypesb

 

Ethiopia

Hospital patients (0.5–80 years)

B (100)

BIII; BIVb

[99]

Ethiopia

Human isolates from urban and rural areas

A (52.5)

 

[164]

  

B (22.0)

  
  

A + F (11.9)

  
  

A + B (13.6)

  

Ghana

Children (≤ 5 years)

B (100)

BIII

[305]

Guinea-Bissau

Children (8.3 months to 7.5 years)

A (11.5)

AII

[309]

  

B (84.6)

  

Kenya

Diarrhoeal children (≤ 5 years)

A (1.4)

AII

[313]

  

B (88.9)

BIII; BIV; BIII/BIVb

 
  

A + B (9.7)

  

Morocco

Urban and rural school children (5–15 years)

A (18.1)

AII

[318]

  

B (81.8)

BIII; BIVb

 

Nigeria

Hospital patients (2 months to 70 years)

A (100)

AII

[166]

Rwanda

Largely asymptomatic children (< 5 years)

A (13.5)

AI; AIIb

[22]

  

B (85.9)

  
  

A + B (0.5)

  

Rwanda

Children (< 5 years)

A (14.0)

 

[24]

  

B (86.0)

  

São Tomé and Príncipe

Children (2 months to 10 years)

A (55.5)

 

[96]

  

B (45.5)

  

Tanzania

Diarrhoeal and non-diarrhoeal outpatients (≤ 71 years)

A (6.7)

 

[340]

  

B (88.8)

  
  

A + B (4.5)

  

Tanzania

Diarrhoeal children and controls (< 2 years)

A (50.0)

 

[72]

  

B (50.0)

  

Tanzania

Primary school children

A (21.4)

AII

[123]

  

B (78.6)

BIII; BIVb

 

Uganda

Individuals living around Kibale National Park

A

AII

[120]

  

B

BIII; BIV

 

Uganda

Apparently healthy children (0–12 years)

A (14.7)

AII

[345]

  

B (73.5)

  
  

A + B (11.8)

  

Uganda

Individuals sharing gorilla habitats

A (100)

 

[163]

aPrevalence (percentage of species identified out of the total number of species genotyped per animal)

bDominant subtype

Table 4

Prevalence and Giardia duodenalis assemblages and subtypes reported in animals from Africa

Country

Animal type

Patient group

Prevalencea

(No. positive/No. tested)

Giardia duodenalis assemblage (Prevalence in %)b

Subassemblage

Reference

Central African Republic

Wildlife

Wild western lowland gorillas (Gorilla gorilla gorilla)

2.0% (4/210)

A (100)

AII

[122]

 

Domestic

Goat (Capra aegagrus hircus)

11.1% (1/9)

E (100)

  

Côte d’Ivoire

Domestic

Dog (Canis familiaris)

54.5% (6/11)

A (33.3)

 

[106]

    

A + B (16.7)

  
    

C (33.3)

  
    

D (33.3)

  
  

Goat (Capra aegagrus hircus)

50% (1/2)

A + B (100)

  
  

Duck (Cairina moschata)

33.3% (1/3)

A + B (100)

  
  

Chicken (Gallus gallus)

58.1% (18/31)

A (38.9)

  
    

B (38.9)

  
    

A + B (22.2)

  

Egypt

Domestic

Cattle (Bos taurus)

6.7% (40/593)

A (15.4)

AI; AII

[80]

    

E (82.7)

  
    

A/E (1.9)

  
  

Buffalo (Bubalus bubalis)

4.7% (10/211)

A (20.0)

  
  

Both cattle and buffalo

53.2% (424/804) by RT-PCR

E (80.0)

  

Egypt

Domestic

Cattle (Bos taurus)

8.7% (4/46)

E (100)

 

[169]

Egypt

Domestic

Calves (Bos taurus)

30.8% (25/58)

A (20.0)

 

[175]

    

E (80.0)

  

Egypt

Wild and cultured

Fish (Tilapia nilotica; Mugil cephalus)

3.3% (3/92)

A (100)

 

[171]

Ghana

Wildlife

Colobus monkey (Colobus vellerosus)

69.2% (74/107)

B (100)

 

[189]

Rwanda

Wildlife

Mountain gorillas (Gorilla beringei beringei)

8.5% (11/130)

B (100)

BIVc; BIII

[124]

 

Domestic

Cattle (Bos taurus)

5.9% (8/135)

E (100)

  

Tanzania

Domestic

Zebus cattle (Bos primigenius indicus)

21.1% (4/19)

A (75.0)

BIV

[123]

    

B (25.0)

  
  

Goats (Capra aegagrus hircus)

22.0% (9/41)

E (66.7)

BIV

 
    

B (22.2)

  
    

A (11.1)

  

Uganda

Wildlife

Gorilla (Gorilla gorilla beringei)

2.0% (2/100)

A (100)

 

[163]

 

Domestic

Cattle (Bos taurus)

10.0% (5/50)

A (100.0)

  

Uganda

Wildlife

Red colobus (Procolobus badius tephrosceles)

11.1%

AII

 

[120]

    

BIV

  
    

E

  
 

Domestic

Livestock (cattle, Bos taurus and Bos indicus, n = 25; goats, Capra aegagrus hircus, n = 57; and sheep, Ovis aries, n = 7)

12.4%

E

  

aPrevalence (percentage of number positive out of the total number of animal species tested)

bPrevalence (percentage of species identified out of the total number of species genotyped per animal)

cDominant subassemblage

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 [102], and eating unwashed/raw fruit [27].

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, 133136]. In Kenya, polyparasitism was more common in patients with diarrhoea than those with single infections of intestinal parasites [137]. 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 [138].

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, 139142] (see Table 2).

Cryptosporidium hominis and C. parvum are the main species infecting humans [6, 143145]. 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, 146154]. 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% [66].

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 [98]. 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 [115] (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 [158160], 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 [141], 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 [89].

Recently a gp60 subtyping assay has been developed for C. viatorum [161], the only species that to date has been found exclusively in humans. A single subtype family, XVa, was identified containing multiple alleles (XVaA3a-XVaA3f) [161]. 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 [161]. 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 [98]. 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) [162]. 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 [148].

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, 163167] (see Table 3). Although many studies have reported that Giardia is not associated with severe diarrhoea [8], one study reported that the prevalence of G. duodenalis Assemblage A was higher among children with vomiting and abdominal pain [22]. Assemblage C was detected in an adult immunocompromised male suffering from bladder cancer and diarrhoea in Egypt [121] and Assemblage F was reported in six diarrhoeal and one asymptomatic individual in Ethiopia [164]. 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, 170173]. However, the majority of research has been conducted on cattle. Prevalence ranging from < 1% in calves [154] to > 86% in calves [174] have been reported for Cryptosporidium and < 6% [123] to > 30% [175] 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 [26].

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 [97], C. erinacei in horses [94] and C. canis in dogs [97]. Cryptosporidium meleagridis was identified in both turkeys and chickens [93, 178] and C. baileyi has been identified in chickens [93]. 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, 139142] (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 [118].
Table 5

Prevalence and Cryptosporidium species and subtypes reported from domesticated animals and wildlife in Africa

Country

Animal type

Animal species

Reported prevalencea

(No. positive/No. tested)

Species (Prevalence in %)b

gp60 subtypes

Reference

Algeria

Domesticated

Turkey (Meleagris gallopavo)

44.6% (25/57)

C. meleagridis (100)

IIIgA18G4R1; IIIgA19G5R1; IIIgA20G4R1; IIIgA21G3R1c; IIIgA24G3R1; IIIgA26G2R1

[93]

  

Chickens (Gallus domesticus)

34.4% (31/90)

C. meleagridis (83.9)

IIIgA18G4R1; IIIgA19G5R1c; IIIgA21G3R1; IIIgA24G2R1; IIIgA26G3R1c

 
    

C. baileyi (16.1)

  

Algeria

Domesticated

Horse (Equus caballus)

2.9% (4/138)

C. erinacei (100)

XIIIaA22R9

[94]

Algeria

Domesticated

Horse (Equus caballus)

2.3% (5/219)

C. parvum (60.0)

IIaA16G1R1c

[100]

    

C. hominis (20.0)

IkA15G1

 
    

C. muris RN66 (20.0)

  
  

Donkey (Equus africanus asinus)

1.6% (2/124)

C. parvum (50.0)

IIaA16G1R1

 
    

C. muris TS03 (50.0)

  

Central Africa Republic

Wildlife

Wild western lowland gorillas (Gorilla gorilla gorilla)

0.5% (1/201)

C. bovis (100)

 

[122]

  

African buffalo (Syncerus caffer)

5.0% (1/20)

C. muris TS03 (100)

  

Côte d’Ivoire

Domestic

Chicken (Gallus gallus)

16.1% (5/31)

C. meleagridis (80.0)

 

[106]

    

C. parvum (20.0)

  

Egypt

Domesticated

Duck (Anas platyrhynchos)

39.9% (365/915)

C. meleagridis (100)

 

[353]

Egypt

Domesticated

Cattle (Bos taurus) and buffalo (Bubalus bubalis)

Cattle: 31.2% (185/593); Buffalo: 35.5% (75/211)

C. parvum (65.7)

IIaA15G1R1; IIdA19G1; IIdA20G1c

[26]

    

C. ryanae (11.8)

  
    

C. bovis (4.1)

  
    

C. parvum + C. ryanae (11.2)

  
    

C. parvum + C. bovis (5.3)

  
    

C. parvum + C. andersoni (1.8%)

  

Egypt

Domestic

Cattle (Bos taurus)

10.2% (49/480)

C. parvum (100)

IIdA20G1

[108]

  

Buffalo (Bubalus bubalis)

12.3% (38/310)

C. parvum (100)

IIdA20G1

 

Egypt

Domestic

Cattle (Bos taurus)

13.6% (269/1974)

C. parvum (43.5)

IIdA20G1; IIaA15G1R1c; IIaA14G1R1r1b

[112]

    

C. andersoni (10.1)

  
    

C. bovis (10.1)

  
    

C. ryanae (18.8)

  
    

Mixed species (17.4)

  

Egypt

Domestic

Water buffalo calves (Bubalus bubalis)

9.5% (17/179)

C. parvum (41.2)

IIdA20Gc; IIaA15G1R1

[111]

    

C. ryanae (58.8)

  

Egypt

Domestic

Calves (Bos taurus)

30.2% (29/96)

C. parvum (92.3)

IIdA20G1c; IIaA15G2R1

[110]

    

C. andersoni (7.7)

  

Egypt

 

Buffalo (Bubalus bubalis)

1.3% (6/466)

C. parvum (33.3)

IIdA20G1; IIaA15G1R1

[113]

    

C. ryanae (66.7)

  
  

Cattle (Bos taurus)

6.9% (31/450)

C. parvum (74.2)

IIdA20G1c; IIaA15G1R1

 
    

C. ryanae (16.1)

  
    

C. bovis (9.7)

  
  

Sheep (Ovis aries)

2.5% (3/120)

C. xiaoi (100)

  

Egypt

Domestic

Cattle (Bos taurus)

10.2% (49/480)

C. parvum (100)

IIdA20G1

[108]

  

Buffalo (Bubalus bubalis)

12.3% (38/310)

C. parvum (100)

IIdA20G1

 

Ethiopia

 

Calves (Bos taurus)

15.8% (71/449)

C. andersoni (76.1)

 

[354]

    

C. bovis (19.7)

  
    

C. ryanae (4.2)

  

Kenya

Domestic

Calves and cattle (Bos taurus)

7.7% (134/1734)

C. parvum-like (68.0)

 

[355]

    

C. ryanae (16.0)

  
    

C. andersoni (12.0)

  
    

C. hominis (4.0)

  

Kenya

Domestic

Cattle (Bos taurus)

Not reported

Cryptosporidium deer-like genotype (100)

 

[177]

Kenya

Wildlife

Olive baboon (Papio anubis)

2.6% (6/235)

C. hominis (100)

IbA9G3c; IIfA12G2c; IiA14

[187]

Madagascar

Domestic

Cattle (Bos taurus)

29.0% (18/62)

C. suis (94.4); Cryptosporidium spp. (5.6)

 

[97]

  

Pig (Sus scrofa)

23.5% (4/17)

C. parvum (75.0); C. suis (25.0%)

  
  

Rodents

33.3% (16/48)

Rat genotype III (31.0); Rat genotype IV (6.3); C. meleagridis (43.8); C. suis (6.3); Unknown (12.5)

  
  

Dog (Canis lupus)

100% (1/1)

C. canis (100)

  
 

Wildlife

Lemur

4.0% (1/25)

C. hominis (100)

  

Nigeria

Domestic

Calves (Bos taurus)

52.3% (34/65)

C. bovis (52.9); C. ryanae (14.7); C. bovis and C. ryanae (32.4)

 

[356]

Nigeria

Domestic

Calves (Bos taurus)

16.0% (31/194)

C. bovis (45.2); C. ryanae (25.8); C. andersoni (16.1); C. bovis + C. ryanae (9.7); C. bovis + C. andersoni (3.2)

 

[85]

Rwanda

Wildlife

Mountain gorilla (Gorilla beringei beringei)

4.0% (4/100)

C. muris (50); C. meleagridis (50.0)

 

[182]

South Africa

Domestic

Calves (Bos taurus)

0.6% (2/352)

C. parvum (50.0); C. bovis (50.0)

 

[154]

South Africa

Domestic

Calves (Bos taurus)

8.0% (4/51)

C. andersoni (50.0); C. bovis (50.0)

 

[90]

 

Wildlife

African buffalo (Syncerus caffer)

2.8% (2/71)

C. ubiquitum (50.0); C. bovis (50.0)

  
  

Impala (Aepyceros melampus)

2.8% (2/71)

C. ubiquitum (100)

  

Tanzania

Wildlife

Baboons (Papio spp.)

10.6% (5/47)

C. hominis (100)

IfA12G2

[102]

  

Chimpanzees (Pan spp.)

19.0% (16/84)

C. hominis (68.8); C. suis (25.0); C. suis and C. hominis (6.2)

IfA12G2

 
 

Domestic

Sheep (Ovis aries)

22.2% (2/9)

C. xiaoi (100)

  
  

Goats (Capra aegagrus hircus)

13.9% (5/56)

C. xiaoi (100)

  

Tunisia

Domestic

Calves (Bos taurus)

21.4% (15/70)

C. parvum (100)

IIaA15G2R1c; IIaA16G2R1; IIaA13G2R1; IIaA20G3R1; IIdA16G1

[114]

Tunisia

Domestic

Sheep (Ovis aries)

11.2% (10/89)

C. bovis (100)

 

[178]

  

Chicken (Gallus gallus domesticus)

4.5% (9/200)

C. meleagridis (100)

  

Tunisia

Domestic

Calves (Bos taurus)

86.7% (26/30)

C. parvum (100)

 

[174]

Uganda

Wildlife

Black-and-white colobus (Colobus guereza;)

3.4% (1/29)

C. parvum (100)

 

[107]

  

Red colobus (Procolobus rufomitratus)

26.7% (8/30)

C. parvum (75.0%); C. parvum/C. hominis/C. cuniculus (25.0)

  
 

Domestic

Goats (Capra aegagrus hircus)

3.5% (2/57)

C. parvum (100)

  

Uganda

Wildlife

Free-ranging mountain gorilla (Gorilla gorilla beringei)

4.0% (4/100)

C. parvum (100)

 

[104]

Zambia

Domestic

Calves (Bos taurus)

34.0% (70/207)

C. parvum (61.9)

 

[118]

    

C. bovis (33.3)

  
    

Cryptosporidium deer-like genotype (4.8)

  

Zambia

 

Goat kid (Capra aegagrushircus)

4.8% (5/105)

C. parvum (100)

 

[117]

  

Lamb (Ovis aries)

12.5% (19/152)

C. parvum (83.3)

  
    

C. suis (16.7)

  

Zambia

 

Calves (Bos taurus)

19.2% (142/744)

C. parvum (64.4)

 

[116]

    

C. bovis (33.3)

  
    

C. suis (2.2)

  

aPrevalence (percentage of number positive out of the total number of animal species tested)

bPrevalence (percentage of species identified out of the total number of species genotyped per animal)

cDominant gp60 subtype

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, 110113] (see Table 5). A unique subtype IIaA14G1R1r1b was also isolated from a calf in Egypt [112]. Cryptosporidium erinacei subtype XIIIa was found in horses from Algeria [94]. 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 [97].

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, 122124, 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 [171].

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 [180], 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 [184] 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 [186].

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 [104]. 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 [90]. Cryptosporidium ubiquitum is considered an emerging zoonotic pathogen [188] 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 [189] (Table 4), again suggesting spill-back. Giardia duodenalis cysts have been found in the faeces of other animals including grasscutters (Thryonomys swinderianus) [190], 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 [191].

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 [192202].

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 [203207], and Tiger nuts (Cyperus esculentus) from Ghana [208]. Cryptosporidium was detected in 16.8% of reared black mussels (Mytilus galloprovincialis) in Mali [209]. 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 [210]. 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 [211]. 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 [214216]. 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 [217], individuals have limited access to privately owned water resources that provide safe water [218]. 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 [218].

Cryptosporidium oocysts and Giardia cysts have been detected in a variety of African water sources including irrigation water in Burkina Faso [219], a stream, well, spring and lake in Cameroon [220, 221], wastewater in Côte d’Ivoire [222], packaged drinking water in Ghana [223225], tap water, drinking water treatment plants, canals, tanks and swimming pools in Egypt [226230]. 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 [235], the surface waters of the Vaal Dam system [236], treated and untreated effluents, sewage, drinking water and roof-harvested rainwater in South Africa [237240]. 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 [218], in piped water in Zambia [243, 244] and wells, springs, tap water and rivers in Zimbabwe [245].

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) [233], 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 [241]. 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 [242]. 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 [2], and the UN Food and Agriculture Organization estimates that 233 million people in sub-Saharan Africa were malnourished in 2014–6 [248]. The ineffectiveness of nitazoxanide in HIV-positive individuals and the contribution of malnourishment to impaired immunity [30], 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 [251], and resistance to all major antigiardial drugs has been reported [252]. Albendazole is also effective in treating giardiasis [251, 253], although its efficacy varies markedly (25–90%), depending on the dosing regimen [254]. Nitazoxanide has been shown to reduce symptom duration in individuals with giardiasis [255] and quinacrine, an old malaria drug, reportedly has 90% efficacy against giardiasis [256], but has potentially severe adverse effects, including a number of psychiatric and dermatologic manifestations [254]. 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 [254].

The prohibitive cost of de novo drug development, estimated to be between $500 million and $2 billion per compound successfully brought to market [257], 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 [254]. 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 [258]. 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 [261]. 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) [262] 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 [263]. 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 [264]. 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% [265]. 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 [268]. 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 [269], 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 [270]. This increase has generally been attributed to poverty, illiteracy, ignorance, big family sizes, climate change, policy and corruption [261].

Conclusions

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.

Abbreviations

AIDS: 

Acquired immunodeficiency virus syndrome

ART: 

Antiretroviral therapy

bg

Beta-giardin

COWP: 

Cryptosporidium oocyst wall protein

ef1-α

Elongation factor 1-alpha

ELISA: 

Enzyme linked immunosorbent assay

gdh

Glutamate dehydrogenase

GEMS: 

Global enteric multicenter study

gp60

Glycoprotein 60

HIV: 

Human immunodeficiency virus

HMG-CoA: 

Human 3-hydroxy-3-methyl-glutaryl-coenzyme A

HSP70: 

Heat shock protein 70

ITS: 

Internal transcribed spacer

LAMP: 

Loop-mediated isothermal amplification

qPCR: 

Quantitative real-time polymerase chain reaction

rDNA: 

Ribosomal deoxyribonucleic acid

RFLP: 

Restriction fragment length polymorphism

rRNA: 

Ribosomal ribonucleic acid

tpi

Triose phosphate isomerase

TRAP: 

Thrombospondin-related adhesive protein

Declarations

Acknowledgements

Not applicable.

Funding

Not applicable.

Availability of data and materials

The data supporting the conclusions of this article are included within the article. Data for this review were sourced from a variety of literature sources including Google Scholar, PubMed, Science Direct, Murdoch University Library (online), Google search and international organization’s websites. Searches were conducted using terms like “Cryptosporidium in Africa”, “Giardia in Africa” and Cryptosporidium or Giardia for each African country in alphabetical order. Searches were also made for information on malnutrition, diagnosis, etc.

Authors’ contributions

Both authors contributed equally to writing the manuscript. Both authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interest.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Not applicable.

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Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
School of Veterinary and Life Sciences, Murdoch University
(2)
Council for Scientific and Industrial Research, Animal Research Institute

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