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Systematic Review

Genetic Diversity of Cryptosporidium Species in Different Hosts in Africa: A Systematic Review

by
Chahari A. Midala
1,
Falmata Kyari
1 and
ThankGod E. Onyiche
1,2,*
1
Department of Veterinary Parasitology and Entomology, Faculty of Veterinary Medicine, University of Maiduguri, PMB 1069, Maiduguri 600230, Nigeria
2
Department of Biological and Environmental Sciences, Faculty of Natural Sciences, Walter Sisulu University, PBX1, Mthatha 5117, South Africa
*
Author to whom correspondence should be addressed.
Parasitologia 2024, 4(4), 405-424; https://doi.org/10.3390/parasitologia4040036
Submission received: 7 November 2024 / Revised: 28 November 2024 / Accepted: 6 December 2024 / Published: 16 December 2024
(This article belongs to the Special Issue The Molecular Epidemiology of Parasites)
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Abstract

:
Cryptosporidium species are protozoan parasites of veterinary and medical importance that infect a wide range of vertebrates globally. Primarily, the mode of infection is typically ingestion of sporulated oocysts, and the risk of transmission to susceptible host is increased by environmental contamination with sporulated oocysts. This systematic review aims to provide a summary of the available data on Cryptosporidium genotypes in Africa. A systematic research of literature on four electronic databases, including Scopus Web of Science, Science Direct, and AJOL, was performed for the determination of Cryptosporidium genotypes in animal and human hosts across Africa between January 2000 to August 2023. All published studies were screened based on the inclusion and exclusion criteria. Overall, 131 Cryptosporidium genotypes were generated from the 47 articles included in this study, which cut across 14 African countries. Cryptosporidium genotypes were reported across all regions within the African continent, such as northern, eastern, western, central, and southern Africa. Cryptosporidium hominis (Ia, Ib, Id, Ie, If, Ih, Ii, and Ik) genotypes were the most dominant, with C. hominis subfamily Ia genotypes reported across all African regions, which indicates high diversity of these subfamilies on the continent. Cryptosporidium parvum (IIa, IIb, IIc, IId, IIe, IIm, and IIi) genotypes were the second dominant genotypes reported, with C. parvum subfamily IIa genotypes having a high diversity across all the African regions with the exception of southern Africa. C. parvum subfamily IIc (IIcA5G3b), which is known to circulate among humans, was reported in a study on dogs in Nigeria. Other documented species of Cryptosporidium with known subtypes in Africa include C. meleagridis (IIIb, IIId, and IIIg), C. cuniculus (Vb), C. ubiquitum (XIIa), C.), and C. erinacei (XIIIa) genotypes. In conclusion, findings from this review have elucidated the Cryptosporidium species and subtypes within the African continent across humans and multiple animal hosts, implying the diversity of this parasites and its ability to infect wide host ranges.

1. Introduction

Cryptosporidium species are intestinal parasites belonging to the phylum Apicomplexa, and they are of both public health and veterinary importance because they infect a wide range of animals, such as birds, carnivores, reptiles, rodents, fishes, marsupials, horses, pigs, ruminants, dugongs, rock hyrax, and humans, globally [1,2,3,4]. The primary mode of infection is typically ingestion of sporulated oocysts, containing four sporozoites. Enterocytes are invaded by sporozoites, which produce parasitophorous vacuoles directly beneath the apical membrane of the enterocyte. Sporozoites go through asexual and then sexual development to produce thick-walled, environmentally resistant oocysts that are discharged into the lumen to facilitate fecal–oral transmission [5,6]. Initial methods for subtyping Cryptosporidium spp. and associated nomenclature relied on DNA sequencing of tandem repeats of the 60-kilodalton(kDa) glycoprotein gene (gp60), encoding surface glycoproteins used in attachment to host cells [7,8]. The species designations (Ia, Ib, etc., for Cryptosporidium hominis; IIa, IIb, etc., for C. parvum; IIIa, IIIb, etc., for C. meleagridis) are used in conjunction with a subtype-specific sequence denoting the number and nature of TCA/TCG/TCT repeats contained within the tandem repeat region [7,8]. For example, the designation, IbA10G2, describes a C. hominis species subtype, having ten TCA and two TCG repeats within the gp60 tandem repeat motif. Globally, the most prevalent C. hominis gp60-subtype families discovered in humans are Ia, Ib, Id, Ie, If, and Ig [9]. Recent advancements in molecular biology have made it possible for the direct ‘typing’ of Cryptosporidium isolates from clinical and environmental samples. Cryptosporidium hominis, C. parvum, C. felis, C. canis, C. meleagridis, and several other Cryptosporidium species/genotypes are now identified as human pathogens, with C. hominis and C. parvum as the dominant species [10]. Cryptosporidium hominis is known to spread within humans, while C. parvum infects both humans and ruminants, with cattle being the major reservoir [11]. Although subtyping C. parvum using DNA sequencing of the gp60 gene has revealed that not all humans infections caused by C. parvum are due to zoonotic transmission because the subtype family IIc is reported to circulate mainly in humans, in contrast to subtype family IIa of C. parvum, which infects ruminants as well as humans [8,12,13]. Numerous studies have also looked at the intraspecific diversity in Cryptosporidium species, mainly focusing on C. parvum and C. hominis, the two main human pathogenic species [10,14,15]. Other studies concerned with understanding the possible transmission routes from the environment and co-habiting animals, such as companion animals and livestock, also reported genotyping at additional genes, which commonly include the 70 kDa heat-shock protein (HSP70), the Cryptosporidium oocyst wall protein (COWP), and the internal transcriber region 1 (ITS-1) [11,16,17,18,19,20,21,22]. Considering the several single-locus genotyping tools reported, those targeting the gp60 gene seem to be the most widely used [23]. The 60 kDa glycoprotein that this gene encodes is post-translationally cleaved to yield the glycoproteins, GP40 and GP15. These glycoproteins are expressed on the surface of sporozoites, where they play a role in the adhesion and invasion of host cells [7,24,25]. Generally, the intraspecific variation in gp60 is accumulated in a highly polymorphic microsatellite region that codes for a serine/threonine stretch in GP40. Generally, the diagnosis and genetic characterization of the different species and population variants (usually recognized as “genotypes” or “subgenotypes”) of Cryptosporidium is central to the prevention, surveillance, and control of cryptosporidiosis [26]. Thus, this systematic review is aimed at summarizing the currently available data on the genetic diversity of Cryptosporidium species from diverse hosts in Africa. This review will also serve as a reference point for One Health scientists within the continent.

2. Materials and Methods

2.1. Search Strategy

This study was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) 2020 guidelines [27,28]. The study protocol was registered in the OSF Registries database, and is available at https://osf.io/d3b6q/?view_only=1abd58cd7f034bd79b9649e26435f68c (accessed on 30 November 2024). The Preferred Reporting Items for Systematic reviews and Meta-Analyses extension for Scoping Reviews (PRISMA-ScR) Checklist is in the Supplementary Materials (Table S1). Literature searches were made for papers published in English between January 2000 and August 2023 on the genetic diversity or subtypes of Cryptosporidium species in Africa from several databases (Scopus, Web of science, Science Direct, and AJOL) were retrieved. The searches in each database were conducted using the Boolean operators “AND” and “OR”. Searches were limited whenever possible to the title, abstract, and keywords. The search strings contained the following search terms (Cryptosporidium OR Cryptosporidiosis) AND (Molecular OR Genotype OR “Genetic Diversity” OR Subtypes) AND (Africa OR Ghana OR Nigeria OR Egypt OR Algeria OR Tunisia OR Madagascar OR South Africa OR Mozambique OR Tanzania OR Morocco OR Kenya OR Uganda OR Sudan OR Togo OR Somali OR Zimbabwe OR Zambia OR Ethiopia OR Gabon OR “Congo OR Cameroon OR “Guinea Bissau OR Gambia OR Lesotho OR Botswana OR Namibia OR “Sao Tome and Principe” OR Senegal).

2.2. Eligibility Criteria

All the selected articles fulfilled the following inclusion criteria: (i) original research article, (ii) written in the English Language only, (iii) cross-sectional study involving the use of molecular based diagnostics principally PCR, (iv) published studies restricted only within Africa, (v) studies reporting Cryptosporidium genotypes and subtypes in humans and animals, (vi) availability of full text for evaluation, and (vii) studies published between January 2000 and August 2023. Studies without the above-listed criteria were all excluded. The exclusion criteria include (i) non-PCR-based studies, (ii) studies that only detect Cryptosporium without genotyping, (iii) articles for which the full text was not retrievable, (iv) studies reporting Cryptosporidium genotypes from other continents, (v) studies published before 2000 and after August 2023, (vi) non-peer-reviewed articles, and (vii) review articles or book chapters.

2.3. Assessment and Selection Process

Articles retrieved from the various databases (Scopus, Web of Science, Science Direct, and AJOL) were exported to Zotero reference manager. The ‘duplicates items’ tab was used to remove duplicate documents. The remaining records were then exported to an Excel spreadsheet and tabulated showing the reference ID, authors, title, periodical, publication year, abstract, notes, publisher, links, and doi of each record. Screening was conducted for relevancy on the remaining records by taking a look at the titles and abstracts. All relevant articles based on titles and abstracts were downloaded for full text evaluation using the eligibility criteria earlier outlined.

2.4. Data Extraction, Quality Assessment and Analysis

Relevant data were extracted from all the eligible studies, and this information includes study characteristics (first author’s name, year of publication and location), methodology (diagnostic technique used), characteristics of subjects (type of host), species, subfamilies, and subtypes of Cryptosporidium reported. These data were tabulated into Excel spreadsheets and descriptively analyzed. Furthermore, a quantitative assessment of methodological quality was undertaken using the Joanna Briggs Institute Critical Appraisal Checklist for Studies Reporting Prevalence Data [29]. Various functions in Excel were used to sort, combine, and visualize the data into tables and charts.

3. Results

3.1. Outcome of the Literature Search

A total of 1417 articles were retrieved after a detailed literature search from 4 databases (Scopus (n = 112), Web of Science (n = 326), Science Direct (n = 836), and AJOL (n = 97)), as shown in Figure 1. Thereafter, 478 duplicate records were removed using Zotero reference manager. Exactly 827 records were removed as unlikely after a careful review of titles and abstracts. A total of 112 articles were downloaded and subjected to full-text assessment. Subsequently, exactly 67 records were excluded (with reasons including n = 39, genotypes not indicated in the results, n = 28, studies not from African continent). A total of 47 articles were used for qualitative synthesis having met the inclusion criteria [30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76] (Table 1).

3.2. Characteristics of All Eligible Studies

Study characteristics of all eligible studies are presented in Table 1. Included studies were published from 2008 to 2022. All studies were conducted in different parts of Africa focusing on Cryptosporidium genotypes reported in humans and animal samples from different countries in Africa. Overall, 139 datasets consisting of 131 unique genotypes were generated from the 47 articles included in this study, which spread across 14 countries that have documented Cryptosporidium genotypes, with Algeria (10/47) [30,31,32,33,34,35,36,37,38,39] having the highest number of studies, followed by Nigeria (8/47) [59,60,61,62,63,64,65,66] and Egypt (7/47) [40,41,42,43,44,45,46]. A detail of the breakdown of eligible studies included in this review per country is presented in Figure 2. Based on the genotyping methods used, 25 studies used nested PCR, followed by PCR-RFLP with 19 studies. A total of 35,568 sample data were obtained, of which 25,535 samples were obtained from humans, and 10,033 samples were obtained from animals. The quality assessment score ranges from 6–8, with the majority of the studies (n = 32) having a score of 8 (Table S2).
Table 1. General characteristics of all the 47 studies included in this study.
Table 1. General characteristics of all the 47 studies included in this study.
CountryHost Spp.Sample SizeCryptosporidium SpeciesSubfamilygp60 SubtypesMolecular TechniquesReference
AlgeriaCamels39Cryptosporidium parvumIfIfA22G2PCR-RFLP[30]
AlgeriaSheep 62Cryptosporidium parvumIIaIIaA13G2R1PCR-RFLP[31]
Goats92Cryptosporidium ubiquitumXIIa
AlgeriaCalves66Cryptosporidium parvumIIaIIaA13G2R1Nested-PCR[32]
AlgeriaChickens and Turkeys147Cryptosporidium meleagridisIIIgIIIgA18G4R1, IIIgA19G5R1, IIIgA20G4R1, IIIgA21G3R1, IIIgA24G2R1, IIIgA24G3R1, IIIgA26G2R1, IIIgA26G3R1PCR-RFLP[33]
AlgeriaChicken, Turkey and Ostrich345Cryptosporidium meleagridisIIIgIIIgA22G3R1, IIIgA23G2R1Nested-PCR[34]
AlgeriaHorsses and donkeys343Cryptosporidium parvumIIaIIaA16G1R1Nested-PCR[35]
Cryptosporidium hominisIkIkA15G1
AlgeriaFishes860Cryptosporidium parvumIIaIIaA16G2R1 IIaA17G2R1Nested-PCR[36]
AlgeriaSheep83Cryptosporidium parvumIIaIIaA21G2R1 IIaA13G2R1Nested-PCR[37]
IIdIIdA16G1
AlgeriaCattle (calves)38Cryptosporidium parvumIIaIIaA16G2R1, IIaA15G2R1Nested-PCR[38]
AlgeriaHorses138Cryptosporidium erinaceiXIIIaXIIIaA22R9Nested-PCR[39]
EgyptRabbits235Cryptosporidium cuniculusVbVbA19,
VbA33		PCR-RFLP[40]
EgyptCalves60Cryptosporidium parvumIIaIIaA15G2R1, IIaA17G3R1, IIaA17G1R1, IIaA19G1R1Conventional PCR[41]
EgyptCalves1974Cryptosporidium parvumIIaIIaA15G1R1PCR-RFLP[42]
IIdIIdA20G1
EgyptCalves29Cryptosporidium parvumIIdIIdA20G1PCR [43]
EgyptCattle and buffalo804Cryptosporidium parvumIIaIIaA15G1R1Nested-PCR[44]
IIdIIdA19G1
Humans165Cryptosporidium parvumIIaIIaA15G1R1
IIaA15G2R1
IIdIIdA20G1
EgyptCattle20Cryptosporidium parvumIIdIIdA20G1Nested-PCR[45]
Buffaloes5Cryptosporidium parvumIIdIIdA20G1
Humans25Cryptosporidium parvumIIdIIdA20G1
EgyptCattle and Buffalo2163Cryptosporidium parvumIIaIIaA15G1R1Nested-PCR[46]
IIdIIdA20G1
EthiopiaHumans520Cryptosporidium parvumIIaIIaA13G2R1, IIaA14G2R1, IIaA15G2R1, IIaA16G2R1, IIaA16G3R1, IIaA17G2R1, IIaA18G2R1, IIaA19G1R1PCR-RFLP[47]
IIbIIbA12
IIcIIcA5G3a
IIdIIdA17G1, IIdA19G1, IIdA22G1, IIdA24G1
IIeIIeA12G1
Cryptosporidium hominisIdIdA20,
IdA24,
IdA26
IbIbA10G2
IeIeA11G3T3
EthiopiaPrimates (monkeys)185Cryptosporidium hominisIaIaA20,
IaA26		Nested-PCR[48]
IblbA10G2
IdIdA21
IeIeA11G3T3
Cryptosporidium parvumIIaIIaA17G1R1, IIaA19G2R1, IIaA15G2R1, IIaA16G1R1, IIaA16G2R1, IIaA17G2R1, IIaA20G1R1
EthiopiaHumans187Cryptosporidium parvumIIaIIaA14G1R1
IIaA15G2R1
IIaA16G1R1
IIaA16G3R1
IIaA17G1R1
IIaA19G1R1
IIaA20G1R1
IIaA22G1R1
IIaA22G2R1		Nested-PCR[49]
IIdIIdA23G1
IIdA24G1
Cryptosporidium hominisIaIaA20
EthiopiaHumans307Cryptosporidium hominisIdIdA17 [50]
IbIbA9G3
CryptosporidiumubiquitumXIIa
GhanaGoats, cattle, sheep and dogs178Cryptosporidium parvumIIcIIcA5G3k [51]
GhanaGoat285Cryptosporidium parvumIIcIIcA5G3qNested-PCR[52]
Sheep and cattle545Cryptosporidium ubiquitumXIIa
GhanaHumans2232Cryptosporidium parvumIIcIIcA5G3a, IIcA5G3b Nested-PCR[53]
IIeIIeA10G1, IIeA10G2
Cryptosporidium hominisIbIbA13G3,
IdIdA15,
IeIeA11G3T3
KenyaCaptive Baboons235Cryptosporidium hominisIfIfA12G2Nested-PCR[54]
IbIbA9G3
IiIiA14
KenyaHumans31Cryptosporidium hominisIIA52G29, IA52G30, IA53G29 IA56G33, IA54G30, IA46G22Nested-PCR[55]
Cryptosporidium parvumIIIIA37G15, IIA36G14, IIA38G15, IIA34G14
KenyaHumans187Cryptosporidium hominisIaIaA25R5, IaA27R3, IaA30R3, IaA7R1PCR-RFLP[56]
IbIbA9G3, IbA9G3R2
IdIdA22,
1dA24,
IdA19,
IdA25,
IdA21,
IdA20, IdA17G1, IdA18, IdA15G1, IdA23GI
IeIeA11G3T3R1, IeA11G3T3
IfIfA19G1, IfA14G1, IfA12G1
Cryptosporidium parvumIIcIIcA5G3R2
MadagascarGoats, cattle, sheep and dogs196Cryptosporidium hominisIbIbA10G2Nested-PCR[51]
IdIdA15G1
MadagascarHumans197Cryptosporidium hominisIbIbA10G2Nested-PCR[76]
MadagascarHumans16Cryptosporidium hominisIaIaA22R3PCR-RFLP[57]
IdIdA15G1
IeIeA11G3T3
Cryptosporidium parvumIIcIIcA5G3
MozambiqueHumans99Cryptosporidium hominisIbIbA10G2Real time PCR[58]
IdIdA22
NigeriaDogs203Cryptosporidium parvumIIcIIcA5G3bNested-PCR[59]
NigeriaHumans285Cryptosporidium parvumIIcIIcA5G3aPCR-RFLP[60]
IIaIIaA15G2R1
NigeriaHumans132Cryptosporidium hominisIaIaA14R3, IaA24R3, IaA27R3PCR-RFLP[61]
IbIbA10G4
IeIeA11G3T3
NigeriaHumans43Cryptosporidium parvumIIcIIcA5G3kPCR-RFLP[62]
Cryptosporidium hominisIaIaA24R3
IbIbA13G3
NigeriaHumans13Cryptosporidium hominisIaIaA30R3 IaA14R3PCR-RFLP[63]
IdIdA11
NigeriaHumans157Cryptosporidium hominisIaIaA23R3, IaA25R3PCR-RFLP[64]
Cryptosporidium parvumIIeIIeA10G1
NigeriaHumans302Cryptosporidium hominisIaIaA18R2, IaA22R2, IaA24R2, IaA25R2, IaA28R2, IaA21R1PCR-RFLP[65]
IbIbA10G2, IbA13G3
IdIdA11,
IdA17
IeIeA11G3T3
IhIhA14G1
Cryptosporidium parvumIIaIIaA15G2R1, IIaA16G1R1
IIcIIcA5G3a, IIcA5G3b
IIiIIiA11
IImIImA14G1
NigeriaHumans394Cryptosporidium hominisIaIaA18R3, IaA25R3, IaA27R4, IaA29R3PCR-RFLP[66]
IbIbA10G2, IbA13G3
IeIeA11G3T3
Cryptosporidium parvumIIcIIcA5G3b IIcA5G3k
IIeIIeA10G1
Sao Tome and PrincipeHumans348Cryptosporidium hominisIaIaA23R3, IaA27R3PCR-RFLP[67]
IeIeA11G3T3, IeA11G3T3R1
Cryptosporidium parvumIIaIIaA16G2R1, IIaA15G2R1
IIdIIdA26G1, IIdA21G1a
South AfricaHumans40Cryptosporidium hominisIaIaA20R3, IaA25G1R3, IaA17R3PCR-RFLP[68]
IbIbA9G3, IbA10G1
IdIdA20,
IdA25,
IdA26,
IdA24
IeIeA11G3T3
IfIfA14G1, IfA12G1
Cryptosporidium parvumIIbIIbA11
IIcIIcA5G3b
IIeIIeA12G1
Cryptosporidium
meleagridis		IIIdIIIdA4
South AfricaHumans8Cryptosporidium hominisIbIbA12G3R2 IbA10G2Nested-PCR[69]
IeIeA11G3T3
SudanCattle149Cryptosporidium parvumIIdIIdA18G1
IIdA19G1		Nested-PCR[70]
TunisiaHumans42Cryptosporidium parvumIIaIIaA14G2R1, IIaA15G2R1, IIaA16G2R1, IIaA20G1R1, Nested-PCR[71]
IIdIIdA15G2R1, IIdA16G2R1, IIdA192R1, IIdA22G2R1,
IIcIIcA5G3
Cryptosporidium hominisIaIaA26G1R1, IaA27G1R1, IaA28G1R1, IaA11G1R1, IaA23G1R1, IaA12R3,
Cryptosporidium meleagridisIIIbIIIbA26G1R1
TunisiaHumans511Cryptosporidium hominisIaIa A11G1R1, Ia A12R3,
IaA23G1R1, IaA26G1R1,
IaA27G1R1,
IaA28G1R1		PCR-RFLP[72]
TanzaniaGoats, cattle, sheep and dogs208Cryptosporidium hominisIfIfA14G1Nested-PCR[51]
IeIeA11G3T3
TanzaniaHumans254Cryptosporidium hominisIfIfA12G2PCR-RFLP[73]
Babboon80Cryptosporidium hominisIfIfA12G2
Chimpanzees251Cryptosporidium hominisIfIfA12G2
TunisiaCattle (calves)15Cryptosporidium parvumIIaIIaA13G2R1, IIaA15G2R1, IIaA16G2R1, IIaA20G3R1Nested-PCR[74]
ZambiaHumans19,033Cryptosporidium hominisIaIaA27R3
IaA30R3		Nested-PCR[75]
IbIbA9G3
IdIdA21
IeIeA11G3T3
Cryptosporidium parvumIIcIIcA5G3a,
IIcA5G3b
IIeIIeA11G1
IIeA12G1
IIsIIsA10G1

3.3. Genetic Diversity of Cryptosporidium Based on Geographical Regions in Africa

The distribution of Cryptosporidium genotypes across the Africa continent according to region is presented below.

3.3.1. Northern Africa

Studies from North African countries, including Algeria, Egypt, Sudan, and Tunisia, account for 27.34% (38/139) of the total number of datasets from this region and 41.9% (55/131) of the overall Cryptosporidium genotypes reported from the continent. Country-wise distribution indicates that studies from Algeria 16.0% (21/131) had the most genotypes, followed by Tunisia 12.9% (17/131), Egypt 11.5% (15/131), and Sudan 1.5% (2/131). These genotypes originated from samples taken from humans (21/55), cattle and buffalo (16/55), sheep and goats (4/55), and domestic and wild birds (10/55). Others, such as rabbits, camel, horse, and fish accounted for the remaining genotypes (4/55). Cryptosporidium species and the documented gp60 subtypes from this region include C. parvum subfamilies (IIa, IIc, IId, and If), C. ubiquitum (XIIa), C. meleagridis with subfamilies (IIIb and IIIg), C. hominis (subfamily Ia and Ik), C. cuniculus (subfamily Vb), and C. erinacei (subfamily XIIa) (Table 2).

3.3.2. Southern Africa

Data from South Africa, Mozambique, and Zambia were used as representation for this region, with four eligible studies [36,51] accounting for 14.4% (20/139) of the dataset from this region and 22.9% (30/131) of the total unique genotypes reported in this study. All Cryptosporidium species genotyped in this region were from humans. Cryptosporidium species reported from this region include C. hominis subfamilies (Ia, Ib, Id, Ie, and If), and C. parvum subfamilies (IIb, IIc, IId, IIe, and IIs) and a C. meleagridis subfamily (IIId) (Table 2).

3.3.3. Eastern Africa

Studies from Eastern Africa (Ethiopia, Kenya, Tanzania, and Madagascar) recorded the highest number of datasets, 30.2% (42/139), as well as having the highest percentage of genotypes, 64.9% (85/131). Country-specific distribution indicates that Ethiopia, 29.0% (38/131), and Kenya, 26.7% (35/131), had the highest percentage of genotypes. Others include Madagascar, 5.3% (7/131), and Tanzania, 3.8% (5/131). Cryptosporidium species gp60 subtypes documented from this region were C. hominis subfamilies (I, Ia, Ib, Id, Ie, If, and Ii), C. parvum subfamily (II, IIa, IIb, IIc, IId, and IIe), and C. ubiquitum (XIIa). Host species from which these genotypes were reported in this region includes humans, 75.3% (64/85), primates, 20.0% (17/85), and other domestic animals, 4.7% (4/85) (Table 2).

3.3.4. Central Africa

Only one study data from Sao Tome and Principe was retrieved for this region, representing 2.9% (4/139) of reported datasets and 6.1% (8/131) of the total genotypes reported in this study. All Cryptosporidium species genotyped were from humans, with Cryptosporidium hominis subfamilies (Ia and Ie) and Cryptosporidium parvum subfamilies (IIa and IId) (Table 2).

3.3.5. Western Africa

A total of eleven studies from West Africa were included in this study, comprising eight (8) studies from Nigeria [59,60,61,62,63,64,65,66] and three (3) from Ghana [51,52,53]. In total, both countries account for 25.2% (35/139) of the total number of datasets and 35.9% (47/131) of the genotypes. With a total of 47 Cryptosporidium genotypes documented, most of the genotypes recorded were from humans (n = 43), while the remaining were obtained from animals such as dogs, sheep, and goats (n = 4). Species recorded and their subtypes were C. parvum subfamilies (IIa, IIc, IIe, Iii, and IIm), C. hominis subfamilies (Ia, Ib, Id, Ie, and Ih), and Cryptosporidium ubiquitum (XIIa). (Table 2).
Table 2. Cryptosporidium species subfamily and gp60 subtypes according to host species.
Table 2. Cryptosporidium species subfamily and gp60 subtypes according to host species.
Host SpeciesSpeciesSubfamilygp60 SubtypeReference
HumansCryptosporidium hominisIIA52G29, IA52G30, IA53G29, IA56G33, IA54G30 IA46G22[55]
IaIaA22R3, IaA23R3, IaA25R3[57,64,67]
IaIaA14R3, IaA24R3, IaA27R3[61,62,75]
IaIaA20R3, IaA25G1R3, IaA17R3[68]
IaIaA30R3, IaA14R3[63,75]
IaIaA26G1R1, IaA27G1R1, [71,72]
IaIaA28G1R1, IaA11G1R1, IaA23G1R1, IaA12R3, [72]
IaIaA18R2, IaA22R2, IaA24R2, IaA25R2, IaA28R2, IaA21R1[65]
IaIaA25R5, IaA27R3, IaA30R3,
IaA7R1		[56]
IaIaA18R3, IaA25R3, IaA27R4, IaA29R3[66]
IaIaA20[49]
IbIbA9G3[50,56,68,75]
IbIbA10G2[47,56,65,69,76]
IbIbA13G3, IbA10G4[53,61,62,66]
IbIbA10G1[68]
IbIbA10G2[58]
IbIbA9G3R2[56]
IbIbA12G3R2[69]
IdIdA20,
IdA25,
IdA26,
IdA24		[47,68]
IdIdA11,
IdA22		[58,63]
IdIdA15,
IdA17		[50,53,65]
IdIdA19,
IdA21,
IdA17G1,
IdA18,
IdA15G1, IdA23GI		[56,75]
IeIeA11G3T3[47,53,57,61,66,68,69,75]
IeIeA11G3T3R1[56,65,67]
IfIfA19G1, IfA14G1, IfA12G1[56,68]
IfIfA12G2[73]
IhIhA14G1[65]
IiIiA37G15, IiA36G14, IiA38G15, IiA34G14[55]
Cryptosporidium parvumIIaIIaA13G2R1, IIaA14G2R1, IIaA15G2R1,
IIaA16G1R1
IIaA16G2R1, IIaA16G3R1, IIaA17G2R1, IIaA18G2R1, IIaA19G1R1, IIaA20G1R1,		[44,47,49,65,67,71,74]
IIaIIaA14G1R1,
IIaA16G1R1,
IIaA17G1R1
IIaA22G1R1
IIaA22G2R1		[44,49]
IIbIIbA11,
IIbA12		[47,68]
IIdIIdA15G2R1, IIdA16G2R1, IIdA19R1, IIdA22G2R1, [71]
IIdIIdA17G1, IIdA19G1, IIdA22G1, IIdA24G1[47,49]
IIdIIdA20G1[44,45]
IIdIIdA26G1, IIdA21G1a[67]
IIdIIdA16G1[74]
IIcIIcA5G3[57,71]
IIcIIcA5G3a,
IIcA5G3b		[47,53,60,65,66,68,75]
IIcIIcA5G3R2[56]
IIeIIeA12G1[47,68,75]
IIeIIeA10G1,
IIeA11G1
IIeA11G2		[53,64,66,75]
IIiIIiA11[65]
IImIImA14G1[65]
Cryptosporidium meleagridisIIIbIIIbA26G1R1[71]
IIIdIIIdA4[68]
CryptosporidiumubiquitumXIIa [50]
CattleCryptosporidium parvumIIaIIaA15G2R1, IIaA17G3R1, IIaA17G1R1, IIaA19G1R1
IIaA15G1R1		[41,42,44,46]
IIaIIaA15G2R1[43]
IIaIIaA13G2R1[32]
IIaIIaA15G2R1, IIaA16G2R1, IIaA20G3R1[38,74]
IIdIIdA18G1
IIdA19G1
IIdA20G1		[43,44,45,46,70]
IIdIIdA16G1
[74]
Cryptosporidium hominisIeIeA11G3T3[51]
Cryptosporidium hominisIfIfA14G1[51]
CryptosporidiumubiquitumXIIa [52]
GoatsCryptosporidium parvumIIcIIcA5G3k
IIcA5G3q		[51,52]
Cryptosporidium hominisIfIfA14G1[51]
Cryptosporidium hominisIeIeA11G3T3[51]
SheepCryptosporidium parvumIIaIIaA21G2R1 IIaA13G2R1[37]
IIdIIdA16G1[37]
CryptosporidiumubiquitumXIIa [52]
DogsCryptosporidium parvumIIcIIcA5G3b[59]
Cryptosporidium hominisIbIbA10G2[51]
IdIdA15G1[51]
CamelsCryptosporidium parvumIfIfA22G2[30]
Domestic/wild BirdsCryptosporidium meleagridisIIIgIIIgA18G4R1, IIIgA19G5R1, IIIgA20G4R1, IIIgA21G3R1, IIIgA24G2R1,
IIIgA22G3R1, IIIgA23G2R1
IIIgA24G3R1, IIIgA26G2R1, IIIgA26G3R1		[33,34]
HorsesCryptosporidium erinaceiXIIIaXIIIaA22R9[39]
Cryptosporidium parvumIIaIIaA16G1R1[35]
Cryptosporidium hominisIkIkA15G1
RabbitsCryptosporidium cuniculusVbVbA19,
VbA33		[40]
BuffaloesCryptosporidium parvumIIdIIdA20G1[45]
FishCryptosporidium parvumIIaIIaA16G2R1 IIaA17G2R1[36]
BabboonsCryptosporidium hominisIbIbA9G3[54]
IfIfA12G2[54,73]
IiIiA14[54]
ChimpanzeesCryptosporidium hominisIfIfA12G2[73]
MonkeysCryptosporidium hominisIaIaA20,
IaA26		[48]
IblbA10G2[48]
IdIdA21[48]
IeIeA11G3T3[48]
Cryptosporidium parvumIIaIIaA17G1R1, IIaA19G2R1, IIaA15G2R1, IIaA16G1R1, IIaA16G2R1, IIaA17G2R1, IIaA20G1R1[48]

4. Discussion

Molecular typing of Cryptosporidium is particularly important for this parasite, as many species are identical morphologically [77]. Molecular identification of species level can be achieved using the following genetic loci: the 18S rRNA, small subunit (SSU) rRNA, heat shock protein 70 (hsp70), actin, and the Cryptosporidium oocyst wall protein gene (COWP) [77]. In the identification of Cryptosporidium species, different types of molecular diagnostic tools have been employed and are categorized into genotyping, subtyping, comparative genomics, and multi-locus typing [78].

4.1. Genotyping of Cryptosporidium

PCR-RFLP is one of the several small subunit (SSU) rRNA-based tools for the identification of Cryptosporidium species. This approach targets the ~830 bp gene fragment and uses VspI, Mboll, and SspI restriction enzymes for genotyping of Cryptosporidium species [79,80]. We documented the widespread use of this approach in several studies involving samples collected from humans, ruminants, and other animals across several regions of the African continent [31,40,47,63,73]. The multi-copy nature of the SSU rRNA gene is responsible for the widespread use of this target for the genotyping of Cryptosporidium. Also, this gene fragment has semi-conserved and hyper-variable regions, which facilitate the design of genus–species primers [1]. We also documented that genotyping of Cryptosporidum species was performed by DNA sequencing of PCR products [35,44,49,51], as well as the utilization of qPCR assays using fluorescent probes in one study involving human samples from Mozambique [58].

4.2. Subtyping of Cryptosporidium

Subtyping has been used extensively in studies involving the transmission of C. parvum in humans and ruminants, C. hominis in humans, and a handful of other related Cryptosporidium species, including C. ubiquitum and C. meleagridis in both humans and animals [9,10,78,81]. The most common subtyping tool for Cryptosporidium species is the DNA sequence analysis of the 60 kDa glycoprotein gene (gp60) [78]. Consequently, all subtyping from all eligible studies was carried out using the gp60 gene, and the wide utilization of this loci is largely due to its polymorphic nature within the Cryptosporidium genome and is under selective pressure and undergoes genetic recombination [81,82]. The genetic heterogeneity in this gene is the variation in the number of a tri-nucleotide repeat (TCA, TCG, or TCT) in the 5′ end (gp40) of the coding region, although extensive sequence polymorphism is also present in the rest of the gene [78]. The latter is employed when defining subtype families within a species, whereas the former is used in identifying subtypes within a subtype family [78]. One important exception of the use of gp60 PCR primers is that it does not amplify DNA of C. ubiquitum and other species that are distant from C. hominis and C. parvum [83,84].
The gp60-based typing system is centered on a combination of tandem serine-coding trinucleotide repeats (TCA, TCG, and TCT) and extensive sequence divergence in non-repeat regions [7,77]. An established subtype nomenclature is used in identifying gp60 subtype family. The nomenclature system starts with a Roman numeral and lower-case letter for each Cryptosporidium and genotype (e.g., C. hominis, Ia, Ib, Id, etc., C. parvum IIa, IIb, IIc, etc.), followed by uppercase letters denoting numbers of repeats. For example, C. hominis subtype IfA19G1R5 has 19 copies of TCA (A) repeats, 1 copy of TCG repeat (G) repeat, and 5 copies of TCT repeats (R) [85]. The trinucleotide repeats (TCA, TCG, TCT) are absent from gp60 genes in C. ubiquitum, C. felis, C. canis, C. ryanae, C. bovis, and C. xiaoi [83,86,87].

4.3. Cryptosporidium hominis

Undoubtedly, C. hominis was the most dominant species in humans across Africa, and this species is known to be transmitted anthropologically. However, we documented the occurrence of C. hominis in animals, including cattle, sheep, goats, dogs, horses, donkeys, and non-human primates [35,48,51,73]. The occurrence of C. hominis in livestock, most importantly ruminants, suggests that they could serve as animal reservoirs, as opined by several authors [88,89,90]. Cryptosporidium hominis subtypes were the most dominant of the genotypes reported in Africa. We did not observe the predominance of any particular C. hominis subtypes. However, C. hominis subfamily Ia recorded the highest frequency across all regions, which indicates high diversity of this subfamily on the continent. Globally, the most prevalent C. hominis subfamilies reported in humans had been documented to belong to the subfamilies: Ia, Ib, Id, Ie, If, and Ig, as reported by Feng et al. [82]. This agrees with the findings of this review, signifying the presence of these subfamilies on the African continent. Furthermore, the occurrence of C. hominis subfamily Ia, Ib, Ie, If, and Ii in non-human primates like baboon, monkeys, and chimpanzees [48,54,73] denotes the potential for zoonotic or anthroponotic transmission. It has been opined that common primate behaviors, such as raiding agricultural fields, homes, and camp food reserves, may increase the likelihood of animal-to-human transmission via infected feces [73]. In Algeria, we observe the occurrence of the Ik C. hominis subtype family in equines, particularly donkeys and horses [35]. This subtype is relatively rare in humans, and the equids are considered as possible reservoir of infection for humans [91,92,93].

4.4. Cryptosporidium parvum

This species is the second most reported genotype documented in this study, and the most important zoonotic species in humans. It has been documented to infect both humans and animals, with cattle being the major reservoir [94]; thus, infected animals may serve as potential reservoirs for human infection. In terms of host range, C. parvum recorded the highest distribution across several animal hosts, including cattle, sheep, goats, fish, buffalo, dog, camel, horses, and monkeys [30,35,36,44,45,51,52,59]. We documented > 30 C. parvum gp60 subtype families with geographic variation in subtype distribution and host adaptation demonstrated. C. parvum subfamily IIa had the highest reported genotypes with a high diversity across all the African regions with the exception of Southern Africa. Its high diversity is of great veterinary and medical importance. C. parvum subfamily IIc genotypes also recorded a high diversity across all the African regions, with the exception of Central Africa. This subfamily IIc was reported to circulate exclusively between humans in contrast to the other subfamilies of C. parvum that infect both humans and animals [12,13,88]; however, in this study, this subfamily IIc (IIcA5G3b) was reported by Ayinmode et al. [59] in dogs in Nigeria. This finding calls for more extensive research in the area of molecular characterization of C. parvum genotypes in animal hosts in order to confirm the diversity of this genotype in dogs and possibly other animal species. A unique subfamily, If-like A22G2 genotype similar to the C. homonis If subfamily was also reported in camels from Algeria [30]. This genotype sequence differed from the sequences of C. hominis If-subfamily in the presence of a 30 bp insertion and 4 SNPs in the non-repeat region [30]. Therefore, more extensive genetic characterization of this unusual C. parvum subtype is needed to fully understand its genetic similarity to C. hominis at the gp60 locus.

4.5. Cryptosporidium meleagridis

This species is commonly found in wild birds but less frequently in poultry. In this study, we documented its occurrence in humans and wild and domestic birds [33,34,68,71]. Phylogenetic evidence suggests that C. meleagridis may originally have been a mammalian parasite that secondarily became established in birds [95]. In humans, subfamily IIIb (IIIbA26G1R1) was documented in Tunisia [74], as well as subfamily IIId (IIIdA4) in South Africa [72]. The other subfamily, IIIg, was reported in domestic and wild birds from Algeria [33,34]. These indicate a low diversity of C. meleagridis genotypes in Africa, which may be due to paucity of research on C. meleagridis genotyping in the African continent.

4.6. Cryptosporidium ubiquitum and Other Species

This species has been reported in humans, cattle, goats, and sheep in Algeria, Ethiopia, and Ghana [31,50,52]. At the gp60 locus, C. ubiquitum lacks the TCA, TCG, and TCT repeats. Of all the eight subtype families (XIIa–XIIh) reported in the literature, only one subtype family, XIIa, has been reported by all the three identified studies in Africa [31,50,52]. It therefore suggests that XIIa is the dominant subtype in Africa. C. erinacei subfamily XIII (XIIIaA22R9) [39] and C. cuniculus subfamily Vb (VbA19, VbA33) [68] were also documented in horses and rabbits, respectively. This also indicates a low genetic diversity of this genotypes, as they were only reported in Algeria and Egypt, respectively (North Africa).

5. Conclusions

This review has established valuable insights into the genetic diversity of Cryptosporidium genotypes across the African continent. Cryptosporidium hominis subfamily Ia and C. parvum subfamily IIa were reported as having the highest diversity in Africa, and the unusual detection of C. parvum subfamily IIc (IIcA5G3b) in dogs in Nigeria underscores the importance of continued surveillance and molecular epidemiology of Cryptosporidium to better understand and mitigate the public health and economic impact of cryptosporidiosis in Africa. Future research should focus more on elucidating on the molecular characterization of Cryptosporidium genotypes, especially in animals, to fully understand the genetic diversity of these parasites on the African content because majority of the genotypes reported in this study were from human hosts compared to animal hosts.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/parasitologia4040036/s1, Table S1: PRISMA 2020 Checklist; Table S2: Quality Assessment Score Checklist.

Author Contributions

Conceptualization, T.E.O. and C.A.M.; methodology, T.E.O. and C.A.M.; validation, T.E.O., C.A.M., F.K. and T.E.O.; formal analysis, C.A.M.; investigation, C.A.M.; resources, C.A.M.; writing—original draft preparation, T.E.O. and C.A.M.; writing—review and editing, T.E.O. and C.A.M.; visualization, T.E.O. and C.A.M.; supervision, F.K. and T.E.O. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Further information on data used in this study can be provided on reasonable request.

Conflicts of Interest

The authors declare no conflicts of interest.

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Parasitologia 04 00036 g001
Figure 1. PRISMA flowchart used in this study for the identification of eligible studies.
Figure 1. PRISMA flowchart used in this study for the identification of eligible studies.
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Figure 2. Summary of Cryptosporidium genotypes reported by countries across Africa.
Figure 2. Summary of Cryptosporidium genotypes reported by countries across Africa.
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Midala, C.A.; Kyari, F.; Onyiche, T.E. Genetic Diversity of Cryptosporidium Species in Different Hosts in Africa: A Systematic Review. Parasitologia 2024, 4, 405-424. https://doi.org/10.3390/parasitologia4040036

AMA Style

Midala CA, Kyari F, Onyiche TE. Genetic Diversity of Cryptosporidium Species in Different Hosts in Africa: A Systematic Review. Parasitologia. 2024; 4(4):405-424. https://doi.org/10.3390/parasitologia4040036

Chicago/Turabian Style

Midala, Chahari A., Falmata Kyari, and ThankGod E. Onyiche. 2024. "Genetic Diversity of Cryptosporidium Species in Different Hosts in Africa: A Systematic Review" Parasitologia 4, no. 4: 405-424. https://doi.org/10.3390/parasitologia4040036

APA Style

Midala, C. A., Kyari, F., & Onyiche, T. E. (2024). Genetic Diversity of Cryptosporidium Species in Different Hosts in Africa: A Systematic Review. Parasitologia, 4(4), 405-424. https://doi.org/10.3390/parasitologia4040036

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