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REVIEW ARTICLE
Cryptosporidium and cryptosporidiosis: the African perspective
Hebatalla M. Aldeyarbi
1,2
&Nadia M. T. Abu El-Ezz
1,3
&Panagiotis Karanis
1,4
Received: 20 January 2016 /Accepted: 22 April 2016
#Springer-Verlag Berlin Heidelberg 2016
Abstract The present overview discusses the findings of
cryptosporidiosis research conducted in Africa and highlights
the currently available information on Cryptosporidium epi-
demiology, genetic diversity, and distribution on the African
continent, particularly among vulnerable populations, includ-
ing children. It also emphasizes the burden of cryptosporidio-
sis, which is underestimated due to the presence of many silent
asymptomatic carriers.
Cryptosporidiosis is recognized as one of the leading
causes of childhood diarrhea in African countries. It has dra-
matic adverse effects on child growth and development and
causes increased mortality on a continent where HIV, poverty,
and lack of sanitation and infrastructure increase the risk of
cryptosporidial waterborne infection.
Keywords Cryptosporidiosis .Africa .Epidemiology
Introduction
Africa leads the world in terms of the disease burden arising
from unclean water and poor sanitation, as almost a quarter of
Sub-Saharan African people lack access to safe drinking wa-
ter, and the number of people lacking basic sanitation has
increased by over 30 % (WHO and UNICEF 2006). Africa’s
high child mortality rate is attributable to this situation. This
high rate is primarily due to infectious diarrhea (11 %), which
is considered the fourth largest child killer after pneumonia,
malaria, and prematurity, particularly in children under the age
of five (WHO 2012). Cryptosporidium is among the top wa-
terborne diseases and is now considered an emerging infec-
tious disease in many parts of Africa (Mor and Tzipori 2008).
Indeed, the importance of Cryptosporidium has increased in
Africa, particularly among vulnerable groups of malnourished
children and immune-compromised individuals, in whom the
disease has a poor prognosis. Large proportions of these vul-
nerable groups consist of children; approximately 500,000 to
700,000 children are infected with HIV each year in Sub-
Saharan Africa (Mahin and Peletz 2009), resulting in the death
of approximately 4 % of these children before the age of five,
with a total HIV/AIDS-specific mortality rate of 160 per 100,
000 persons in the African region (WHO 2012). Climate
change will exacerbate the pressures exerted on water avail-
ability, accessibility, and demand, further emphasizing the
potentially increasing threat of waterborne infectious
diseases. Jagai et al. (2009) have provided a quantitative link
between the incidence of cryptosporidiosis and meteorologi-
cal parameters on a global scale, particularly in warm and wet
areas of Africa.
In this paper, we attempted to establish a special BAfrican
Cryptosporidium database^to compile sound information on
Cryptosporidium infection and epidemiology with respect to
Responsible editor: Philippe Garrigues
*Hebatalla M. Aldeyarbi
heba_deyarbi@daad-alumni.de
1
Center for Anatomy, Institute I, University of Colognem,
Joseph-Stelzmann-Street 9, 50937 Cologne, Germany
2
Present address: Department of Parasitology, Faculty of Medicine,
Suez Canal University, Ismailia 41522, Egypt
3
Present address: Parasitology and Animal Diseases Department,
National Research Centre, Dokki, Cairo, Egypt
4
Present address: Thousand Talents Plan of the Chinese Government,
Center for Biomedicine and Infectious Diseases, Qinghai Academy
of Animal Science and Veterinary Medicine, Xining, China
Environ Sci Pollut Res
DOI 10.1007/s11356-016-6746-6
transmission of this disease in African countries and the urgent
need for an effective intervention on this continent.
Cryptosporidiosis risk factors
Waterborne cryptosporidiosis in Africa
Waterborne cryptosporidiosis and outbreaks are more com-
monly reported; up to the end of 2010, a total of 185 outbreaks
were reported worldwide (Karanis et al. 2007; Baldursson and
Karanis 2011). This information is in contrast with the odd
observation that no outbreaks have been reported in Africa to
date, raising numerous questions and hypotheses including
the following: is Africa free of Cryptosporidium outbreaks?
However, an increasing number of studies have demon-
strated that Cryptosporidium oocysts are present in different
bodies of water, including lakes, rivers, sewage, treated efflu-
ents, and drinking water, in several African countries, suggest-
ing the potential for endemic waterborne Cryptosporidium
transmission. These bodies of water include a eutrophic lake,
stream, and effluent waters in Cameroon (Ajeagah et al.
2007), municipal drinking water in Ethiopia (Fikrie et al.
2008), and drinking water treatment plants, tanks, canals,
and swimming pools in Egypt (Youssef et al. 1998; Ali et al.
2004; Rayan et al. 2009). C. parvum and C. andersoni isolates
in the Njoro watershed (Muchiri et al. 2009), the Kathita and
Kiina rivers in Kenya (Kato et al. 2003), well water, the Kano
river in Nigeria (Uneke and Uneke 2007), the surface waters
of the Vaal Dam, treated effluents, drinking water in South
Africa (Kfir 1995; Dungeni and Momba 2010), and piped
water in Zambia (Kelly et al. 1997;Nchitoetal.1998) all have
been found to be contaminated with Cryptosporidium oocysts.
Considering that a dose of less than ten oocysts is sufficient to
cause infection in humans, cryptosporidial waterborne infec-
tions from such waters are expected.
The main challenge is addressing threats to surface water
attributed to the hazardous habits of native people, as well as
to poor living conditions and services. The major sources of
water pollution include uncontrolled sewage discharges, poor-
ly managed wastewater treatment plants (Ajeagah et al. 2007;
Dungeni and Momba 2010), and contaminated runoff water
from densely populated areas, and unsanitary settlements
lacking infrastructure along rivers (Uneke and Uneke 2007).
Cryptosporidium oocysts have been identified in the feces of
many animals, such as calves (Siwila et al. 2007;Salyeretal.
2012; Helmy et al. 2013), domestic livestock (Soltane et al.
2007), horses (Laatamna et al. 2013), and birds, including
broiler chickens, quail, and ostriches (Penrith et al. 1994;
Soltane et al. 2007; Shaapan et al. 2011). In addition, different
wild animals that could also be considered potential sources of
infection have been reported to harbor Cryptosporidium spe-
cies (Abu Samra et al. 2011; Salyer et al. 2012). Considering
that water bodies in Africa are shared by humans and domes-
ticated and wild animals, the risk of surface water contamina-
tion via the shedding of Cryptosporidium from these entities is
greatly increased. The fact that isolates from humans and an-
imals can survive over time in all environmental waters is
likely reflected by the extensive health threat to the local pop-
ulations associated with the use of such receiving water bodies
for drinking, recreational, and agricultural purposes (Ajeagah
et al. 2007; Muchiri et al. 2009;DungeniandMomba2010)
when the quality of the water bodies and piped water supplied
to homes is unsafe, poor or otherwise unacceptable for human
consumption (Obi et al. 2002).
Clearly, much hinges on the frequency of waterborne cryp-
tosporidiosis, as individuals are infected via the consumption
of water from different sources in different countries (Kelly
et al. 1997;Nchitoetal.1998; Adjei et al. 2004; Morse et al.
2007; Uneke and Uneke 2007; Adamu et al. 2010;Akinbo
et al. 2010; Tigabu et al. 2010; El-Helalya et al. 2012; Salyer
et al. 2012). For example, ponds, rivers, wells, and tap water in
Ghana (Adjei et al. 2004), tap water in Egypt (El-Helalya et al.
2012), springs, wells, tap water, and dam water in Ethiopia
(Ayalew et al. 2008; Adamu et al. 2010; Tigabu et al. 2010),
rivers, and unprotected wells in Malawi (Morse et al. 2007),
streams/rivers, well water, and underground tanks in Nigeria
(Uneke and Uneke 2007; Akinbo et al. 2010;Maikaietal.
2012), rivers, non-chlorinated wells, treated effluents, and
final-treated water samples in South Africa (Kfir 1995), open
water sources (e.g., ponds or streams) in Uganda (Salyer et al.
2012), and piped water in Zambia (Kelly et al. 1997;Nchito
et al. 1998)havebeenreportedtobecontaminatedwiththis
pathogen. Indeed, the high Cryptosporidium spp. contamina-
tion levels in river water, irrigation water in Kumasi, Ghana,
and vegetables consumed raw highlight a potential risk of
cryptosporidiosis (Petersen et al. 2014).
The high burden of endemic diarrhea among Kenyan chil-
dren aged less than 2 years, particularly those drinking river
water (22 %) compared to other types of water (8–11 %),
supports the possibility of waterborne Cryptosporidium trans-
mission (Tiwari and Jenkins 2008). Detection of the Ia
C. hominis subtype family in a 10-month-old malnourished
Nigerian child was linked to a well that was used as a source
of drinking water (Maikai et al. 2012). Ib, Ie, the
anthroponotic IIc, and two new subtype families of
C. parvum were recovered from Nigerian patients who used
streams, rivers, and boreholes (Akinbo et al. 2010), all sug-
gesting waterborne transmission. In addition, a survey was
carried out by Kelly et al. (1997)inZambiatoestablishthe
prevalence of persistent cryptosporidial diarrhea in 1995 by
studying oocyst cryptosporidial contamination in water
sources. The results of this survey demonstrated a clear and
significant relationship between water contamination and in-
fection in 16 out of 506 adults who had diarrhea during the
2 weeks prior to the study.
Environ Sci Pollut Res
Climate, meteorology, and cryptosporidiosis in Africa
It appears that cryptosporidiosis infection is characterized
by a low endemic level and highly pronounced seasonal
outbursts, signifying the strong effects of meteorological
and environmental factors (Jagai et al. 2009). Many studies
conducted in Africa have confirmed and expanded upon
the observation of Ba marked seasonal variation in the rate
of Cryptosporidium detection^(Gatei et al. 2002;Morse
et al. 2007;Ayalewetal.2008; Jagai et al. 2009;Adamu
et al. 2010; Creek et al. 2010; Tigabu et al. 2010), ultimate-
ly leading to the conclusion that under certain environmen-
tal conditions, Cryptosporidium can make its way into sur-
face waters and survive there to become a waterborne path-
ogen. Contamination of surface water sources undoubtedly
increases during rainy seasons due to runoff containing
feces from both infected animals and humans (Gatei et al.
2002; Morse et al. 2007;Ayalewetal.2008; Adamu et al.
2010; Creek et al. 2010;Tigabuetal.2010). Indeed, this is
an inevitable phenomenon in some African countries such
as Botswana, where breakdown in the sanitation infrastruc-
ture, poor hygiene, and the use of unprotected water
sources in association with heavy rainfalls cause diarrheal
outbreaks and mortality among children less than 5 years
old (Creek et al. 2010).
In Sub-Saharan Africa, increasing temperatures and precip-
itation are predictive of an increasing incidence of cryptospo-
ridiosis. Analysis performed in a previous study adjusting for
distance from the equator has revealed that moist tropical lo-
cations, such as Burkina Faso, Gabon, Gambia, Guinea
Bissau, Kenya, Malawi, Rwanda, and Uganda, experience
strong precipitation-associated seasonal fluctuations in the
cryptosporidiosis incidence (Jagai et al. 2009). Further,
Muchiri et al. (2009) have reported contamination of the
Meru surface waters in Kenya with Cryptosporidium at the
end of the rainy season. In fact, a relationship between human
cryptosporidiosis infection during the rainy and warm seasons
has been noted in many African studies (Kfir 1995; Kelly et al.
1997;Nchitoetal.1998; Amadi et al. 2001;Pengetal.2003;
Tumwine et al. 2003; Morse et al. 2007; Ayalew et al. 2008;
Molloy et al. 2010; Siwila et al. 2011; Salyer et al. 2012). Jagai
et al. (2009) developed a meta-analysis framework to assess
the link between environmental exposure to protozoa via
drinking and recreational water and cryptosporidiosis
infection. They confirmed the results of previous studies and
noted a marked increase in cryptosporidiosis infection during
warm and rainy seasons. King and Monis (2007)havesug-
gested that the oocysts can persist in the environment and be
readily mobilized by precipitation events, which might result
in a significantly increased risk.
However, peak Cryptosporidium transmission coincid-
ingwiththehotanddryseasonsandextendingintoearly
autumn has also been reported (Bogaerts et al. 1987;
Wittenberg et al. 1987; Fripp et al. 1991; Gatei et al.
2006; Adamu et al. 2010;Molloyetal.2010; Nel et al.
2011; Abd El Kader et al. 2012). This could be attributed to
poor hygiene as a consequence of water shortages during
these dry months or the use of alternative water sources,
such as wells, which may harbor high oocyst concentra-
tions(Gateietal.2006). On the other hand, some studies
have failed to find a correlation between the incidence of
Cryptosporidium and climatic factors, suggesting that oth-
er factors, such as personal hygiene, the potable water sup-
ply, and sanitation, have more significant impacts than wa-
terborne transmission (Jarmey-Swan et al. 2001).
Regardless, no study to date has examined the seasonal
patterns and distributions of different Cryptosporidium
species in Africa; thus, these aspects remain to be
evaluated.
Airborne transmission of Cryptosporidium spp.
and extra-intestinal infection in Africa
Respiratory cryptosporidiosis, which is well established in
birds, has also been documented in patients with diarrhea
and/or respiratory symptoms in Africa. Reports of
cryptosporidial infections of the respiratory tract (Bogaerts
et al. 1987; Wittenberg et al. 1987; Fripp et al. 1991;Mor
et al. 2010;Talietal.2011;El-Helalyaetal.2012) and biliary
tract (Liong and Sukumar 2009), as well as gastric cryptospo-
ridiosis (Kourda et al. 2008), among immune-deficient and
immune-competent Africans have indicated that this protozo-
an is not restricted to the gastro-intestinal tract but rather ex-
hibits extraintestinal tropism.
Respiratory cryptosporidiosis has been identified in
immune-competent individuals (Bogaerts et al. 1987;
Wittenberg et al. 1987; Fripp et al. 1991; Mor et al. 2010),
as well as in a Moroccan patient with late-stage AIDS (Tali
et al. 2011). Oocysts have also been detected in the sputum of
an 84-year-old male South African patient presenting only
with a persistent productive cough and an inverted
CD4:CD8 ratio (Fripp et al. 1991) and in a Rwandese adult
with bronchopulmonary cryptosporidiosis (Bogaerts et al.
1987). Further, Mor et al. (2010) detected respiratory crypto-
sporidiosis in one-third of HIV-seronegative Ugandan chil-
dren with intestinal cryptosporidiosis, 59 % of whom had a
normal nutritional status. This group identified C. hominis and
C. parvum as the only respiratory pathogens in 12 children
with respiratory cryptosporidiosis out of a total of 17 children.
The onset of cough before diarrhea was reported in 29.4 % of
the children with respiratory cryptosporidiosis, suggestingthat
airborne transmission of Cryptosporidium occurred via inha-
lation of droplets containing oocysts, thereby causing respira-
tory tract infection and gastroenteritis. These findings high-
light the potential for respiratory transmission among
immune-competent persons.
Environ Sci Pollut Res
The risk of Cryptosporidium infection in travelers to Africa
Another key issue that is noteworthy is that individuals trav-
elling to developing countries are more prone to travel-related
diarrhea. Cryptosporidiosis has been reported among several
groups of travelers, including infants and tourists returning
from Egypt, the island of Mauritius, Nigeria, Tunisia, and
West Africa (Soave and Ma 1985; Ungar et al. 1989;Gatti
et al. 1993;Chalmersetal.2008; Agnamey et al. 2010).
Serologic evidence of Cryptosporidium infection has been
demonstrated in Peace Corps volunteers serving in West
Africa; 14 % became newly IgG positive (8/56) during their
first year, and 13.6 % (3/22) became positive over a 2-year
period (Ungar et al. 1989). Agnamey et al. (2010)alsoreport-
ed a case of chronic diarrhea due to C. hominis in a 1-year-old
child returning from West Africa; this child was Guinean and
exhibited signs of severe dehydration and weight loss. Similar
events have been described in three infants, including one
child aged 3 years and two adult members of two families,
after their return from traveling to the African continent
(Soave and Ma 1985). Further, a patient returning from
Kenya was found to be infected with an IaA25R3 subtype
(Chalmers et al. 2008) that was identical to the C. hominis
subtype found in Nigeria (Akinbo et al. 2010, Maikai et al.
2012). Therefore, travelling abroad is regarded as a risk factor
for cryptosporidiosis, particularly traveling to countries where
consumption of contaminated water or foods with
Cryptosporidium occurs more frequently.
Cryptosporidium and vulnerable groups in Africa
Cryptosporidiosis in children and adults
A review of pediatric cryptosporidiosis in Sub-Saharan Africa
was published by Mor and Tzipori (2008), including research
outcomes, while the present review is focused on studies con-
ducted in different regions of Africa and highlights the ongo-
ing importance of Cryptosporidium on this continent.
Studies conducted between 1985 and 2014 in different
countries in Africa have confirmed the growing importance
of Cryptosporidium infection as a major cause of human di-
arrheal illness. In Africa, the transmission of Cryptosporidium
within households, schools (Højlyng et al. 1986; Ayalew et al.
2008), and hospital environments (Peng et al. 2003; Tumwine
et al. 2003; Essid et al. 2008; Creek et al. 2010;Talietal.
2011), as well as nosocomial outbreaks of cryptosporidiosis,
have been reported (el-Sibaei et al. 2003). It is recognized as
one of the leading causes of moderate-to-severe diarrhea in
children in Sub-Saharan African and African Mediterranean
countries, particularly in children younger than 5 years of age
(Soave and Ma 1985; Højlyng et al. 1986; Bogaerts et al.
1987; Walters et al. 1988; Fripp et al. 1991; Nchito et al.
1998; Amadi et al. 2001;Banwatetal.2003; Tumwine et al.
2003; Adjei et al. 2004; Gatei et al. 2006; Morse et al. 2007;
Ayalew et al. 2008;MorandTzipori2008; Mor et al. 2009,
2010; Creek et al. 2010;Molloyetal.2010; Opintan et al.
2010; Siwila et al. 2010; Tigabu et al. 2010; Ben Abda et al.
2011; Nel et al. 2011; Abd El Kader et al. 2012; El-Helalya
et al. 2012;Maikaietal.2012). In spite of the wide array of
putative pathogens, Cryptosporidium hasbeenrecognizedas
a significant pathogen in four Sub-Saharan African countries,
regardless of the HIV prevalence, and as the second most
common pathogen in infants (Kotloff et al. 2013).
Remarkably, infection can be acquired before the age of 1 year
(Højlyng et al. 1986; Fripp et al. 1991;Nchitoetal.1998;
Peng et al. 2003; Adjei et al. 2004; Gatei et al. 2006;Morse
et al. 2007; Opintan et al. 2010;Maikaietal.2012), particu-
larly among infants and toddlers attending daycare centers in
Africa (Walters et al. 1988; Siwila et al. 2010). It is likely that
transmission of a small infective dose via the airborne route
(Højlyng et al. 1987), or hand-to-mouth route, or an unsafe
water supply (see Section 2, and Fig. 1) may play an important
role in development of this infection in these infants.
The results of many African studies have indicated that
immune-compromised patients, particularly HIV-infected in-
dividuals with a low CD4 cell count who are at risk of cryp-
tosporidiosis, account for almost 50 % of cases (Bogaerts et al.
1987; Kelly et al. 1997;Mwacharietal.1998; Amadi et al.
2001;Pengetal.2003; Adjei et al. 2004; Houpt et al. 2005;
Tumwine et al. 2005;Akiyoshietal.2006; Samie et al. 2006;
El-Hamshary et al. 2008;Assefaetal.2009; Mor et al. 2009;
Ben Abda et al. 2011; Nel et al. 2011; Ojurongbe et al. 2011;
Tali et al. 2011; Wumba et al. 2012). The HIV epidemic in
Sub-Saharan Africa has resulted in an enhanced burden of
Fig. 1 Cryptosporidiosis and routes of transmission
Environ Sci Pollut Res
cryptosporidiosis due to increased susceptibilities to opportu-
nistic parasites and intestinal infection at later stages of HIV
infection, when enteropathy supervenes (Kelly et al. 1997,
Assefa et al. 2009). Indeed, persistent Cryptosporidium infec-
tion could be a marker of advanced AIDS (Bogaerts et al.
1987, Tumwine et al. 2005) in the absence of antiretroviral
therapy (ART) (Wumba et al. 2012) or even with this therapy
(Nel et al. 2011). Intriguingly, a low CD4 cell count has been
demonstrated to be a distinguishing feature of asymptomatic
HIV patients (Houpt et al. 2005, Sarfati et al. 2006) receiving
antiretroviral therapy (Sarfati et al. 2006). Additional analyses
are required to evaluate the significance of this observation.
Cryptosporidium has been found to account for a considerable
proportion of chronic diarrhea cases among AIDS patients in
Africa (Assefa et al. 2009).
Cryptosporidiosis, malnutrition, and breastfeeding
In many studies, bottle feeding (non-breastfeeding) or
weaning are considered risk factors for cryptosporidiosis in
children less than 18 months of age (Højlyng et al. 1986;
Creek et al. 2010). It is believed that breastfeeding might
provide some protection against infection, particularly for
those children who are exclusively breastfed (Højlyng et al.
1986; Tumwine et al. 2003; Adjei et al. 2004; Creek et al.
2010), given that infant formula is not always sustainable or
safe in a population in which the water quality varies substan-
tially with changes in the weather (Creek et al. 2010).
Contrary to this common belief, cryptosporidiosis was detect-
ed in African children fed breast milk who did not demon-
strate decreased susceptibility to infection (Nchito et al. 1998;
Tumwine et al. 2003; El-Helalya et al. 2012; Maikai et al.
2012). It is possible that breastfeeding might be associated
with a higher HIV seroprevalence, thereby increasing the
cryptosporidiosis risk in these children (Nchito et al. 1998).
Moreover, the failure of breastfeeding to prevent
Cryptosporidium infection in children whose mothers have
demonstrable breast milk antibodies against this parasite has
also been documented (Højlyng et al. 1987). Indeed, the high
rates of seroconversion to Cryptosporidium shortly after birth
in Bedouin infants who originated from various locations,
including the Middle East and North Africa (Robin et al.
2001), indicate a large amount of natural exposure to this
protozoan.
Notably, an increasing number of African studies have
linked persistent diarrhea (PD) to cryptosporidiosis and mal-
nutrition, which cause further deterioration of the infected
child’s condition (Bogaerts et al. 1987; Amadi et al. 2001,
Tumwine et al. 2003,2005; Adjei et al. 2004; Morse et al.
2007; Mor et al. 2009,2010; Creek et al. 2010; Opintan et al.
2010; Ben Abda et al. 2011; Nel et al. 2011; El-Helalya et al.
2012; Maikai et al. 2012). The exact degree to which malnu-
trition and diarrhea are associated with cryptosporidiosis is not
known; however, they are assumed to have a complex bidi-
rectional relationship (Opintan et al. 2010). In many African
studies, a poor nutritional status has been found to be a deter-
mining factor for Cryptosporidium infection with a less favor-
able outcome (Bogaerts et al. 1987; Tumwine et al. 2003,
Creek et al. 2010). Notably, a correlation between early child-
hood cryptosporidiosis and growth reduction or even failure
has been identified (Checkley et al. 1997; Tumwine et al.
2003; Mor et al. 2009), particularly in children younger than
12 months (Lorntz et al. 2006), in addition to long-term cog-
nitive deficits and impaired physical fitness later in life
(Guerrant et al. 1999;Lorntzetal.2006). Moreover, if cryp-
tosporidiosis is present along with another infection, such as
microsporidiosis and/or HIV, then the growth rate may be
even lower (Mor et al. 2009). Furthermore, stunting might
have an additional effect on childhood intellectual function,
independent of the effects of diarrhea (Pinkerton et al. 2008).
Therefore, Basymptomatic^cryptosporidiosis can have dra-
matic adverse effects on child growth and development into
later childhood (Checkley et al. 1997). Asymptomatic crypto-
sporidiosis has been identified in Zambian children attending
daycare (28.0 %) (Siwila et al. 2010), and two other studies
(Siwilaetal.2007; Ayalew et al. 2008) have determined that a
proportion of all Cryptosporidium spp.-infected individuals
are asymptomatic (6 and 12.2 %, respectively), highlighting
the presence of asymptomatic patients in Africa. Surprisingly,
Banwat et al. (2003) found that their control group only ex-
creted Cryptosporidium oocysts (3.8 %) compared to a study
group of malnourished children with HIV (0 %). This finding
might be related to immune reconstitution by highly active
antiretroviral therapy (Maggi et al. 2000). However, this ob-
servation clearly needs to be further investigated.
Analyses conducted in other African studies have not re-
vealed large disparities between symptomatic children with
diarrhea and asymptomatic children, as the differences in
prevalence have ranged from 0.5 to almost 7 % (Højlyng
et al. 1986; Jarmey-Swan et al. 2001; Opintan et al. 2010).
However, the prevalence has reached as high as 40 % (Siwila
et al. 2011). These findings emphasize the lack of correlation
between disease severity or symptoms and Cryptosporidium
infection that may persist beyond the clinical illness. The high
long-term rate of excretion of Cryptosporidium oocysts persists
for almost 2 months after symptoms subside, and it is
thought to be attributable to relative immune-incompetence
(Walters et al. 1988), but this remains to be confirmed.
In addition, no data are available on the prevalence of
asymptomatic carriage among adult populations in Africa.
Houpt et al. (2005) and Jarmey-Swan et al. (2001)havesug-
gested that asymptomatic cryptosporidial infection is under-
appreciated, at least in some regions of Africa. The reported
asymptomatic adult cases, which contribute to the silent dis-
semination of infection in the environment, have reached ap-
proximately 45 % (Inabo et al. 2012; Salyer et al. 2012). It
Environ Sci Pollut Res
appears that the extent of infection is underestimated, presum-
ably due to the use of less-sensitive methods, such as micros-
copy, compared to molecular techniques.
Despite the improving trends in reducing the mortality rate
of children under 5 years old, in 2010, an estimated 57 deaths
occurred per 1000 live births. The annual rate of decrease in
the WHO African Region, where almost half of all child
deaths occur, increased from 1.8 to 2.8 % from 1990–2010.
In Mediterranean African countries, the diarrheal mortality
rate in children under five was between 1 % (in Libya) and
12 % (in Sudan) in 2010, whereas in Sub-Saharan Africa, it
ranged from 5 % in South Africa to 16 % in Somalia (WHO
2012). According to the World Health Report in 1996,
Cryptosporidium was named one of the diarrhea-causing in-
fectious agents responsible for millions of deaths in 1995
(Holden 1996). Some authors have speculated that there is a
significant association between cryptosporidiosis and both
failure to thrive during childhood and Cryptosporidium-asso-
ciated diarrheal deaths, particularly in adult HIV patients
(Amadi et al. 2001). An association of Cryptosporidium with
a higher risk of death in toddlers aged 12–23 months with
moderate-to-severe diarrhea (4 %) during the ensuing 2–
3 months was emphasized in a case/control Global Enteric
Multicenter Study (GEMS) conducted in Sub-Saharan
Africa (Kenya, Mali, Mozambique, and Gambia) and in
South Asia (Kotloff et al. 2013). This high risk of death could
be a consequence of acute severe or persistent diarrhea, severe
dehydration, electrolyte disturbances, pneumonia, septicemia,
malnutrition, or an underlying immune-compromised status,
which could result in deterioration of the patient’sconditionor
lengthy hospitalization (Wittenberg et al. 1987; Amadi et al.
2001;Leavetal.2002; Tumwine et al. 2003;Konateetal.
2005; Creek et al. 2010; Nel et al. 2011;Talietal.2011); this
could also be the result of failure to manage diarrhea, dehy-
dration, or malnutrition or simply due to inefficient and inap-
propriate treatment (Tumwine et al. 2005;Akiyoshietal.
2006; Creek et al. 2010). Indeed, Cryptosporidium has been
reported to be the single most significant predictor of death in
HIV-seropositive patients (Mwachari et al. 1998; Amadi et al.
2001) and an indicator of morbidity and mortality in children
(Wittenberg et al. 1987).
Molecular epidemiology of cryptosporidiosis
in Africa
Despite the high prevalence of cryptosporidiosis in develop-
ing countries, genetic characterization of Cryptosporidium
species is lacking, particularly in Africa, and few molecular
and epidemiological studies have been conducted. C. hominis,
C. parvum, C. canis,C. felis,C. meleagridis,C. muris,the
C. muris Brock hyrax^isolate and the C. muris Bcalf^isolate
C. andersoni,C. cuniculus, aCryptosporidium rabbit
genotype, a Cryptosporidium cervine genotype, and
C. serpentis have been reported, indicating an increase in the
diversity of species causing human cryptosporidiosis (Morgan
et al. 2000;Pengetal.2001,2003; Gatei et al. 2002,2003,
2006;Leavetal.2002; Tumwine et al. 2003,2005; Houpt
et al. 2005;Akiyoshietal.2006; Samie et al. 2006;Morse
et al. 2007;Siwilaetal.2007; El-Hamshary et al. 2008;Essid
et al. 2008;Blancoetal.2009;Eidaetal.2009; Adamu et al.
2010;Akinboetal.2010; Creek et al. 2010;Molloyetal.
2010; Mor et al. 2010; Ben Abda et al. 2011; Abd El Kader
et al. 2012; Ayinmode et al. 2012;Maikaietal.2012; Salyer
et al. 2012; Helmy et al. 2013). Indeed, the presence of various
species of Cryptosporidium in human infections indicates that
both anthroponotic and zoonotic transmission cycles are po-
tential in the infection of humans. However, a separate sylvat-
ic transmission cycle exists in some protected areas (Salyer
et al. 2012). Despite the dearth of data on the prevalence of
Cryptosporidium in wild animals, it appears that
Cryptosporidium spp. are circulating in wildlife populations
and should be considered essential contributors to environ-
mental pools of this parasite that threaten humans (Salyer
et al. 2012, Abu Samra et al. 2011).
Regardless of the immune status, the C. hominis species
has been found to be the predominant species infecting
humans in many African studies (Morgan et al. 2000; Peng
et al. 2001,2003; Gatei et al. 2003,2006; Tumwine et al.
2003,2005; Houpt et al. 2005;Akiyoshietal.2006;Samie
et al. 2006; Morse et al. 2007;Akinboetal.2010;Molloy
et al. 2010; Mor et al. 2010; Ben Abda et al. 2011;AbdEl
Kader et al. 2012;Maikaietal.2012; Helmy et al. 2013), and
these infections could be attributed to direct or indirect
anthroponotic transmission. Interestingly, the rabbit genotype,
which was found in Nigeria (Molloy et al. 2010), is closely
related to C. hominis,withRFLPpatternsatthe
Cryptosporidium oocyst wall (COWP) locus sharing 99.2
and 99.7 % similarity at the 18S and heat-shock protein
(HSP) loci, respectively (Rayan et al. 2009). Thus, it is not
surprising that the rabbit genotype was detected in twins, in-
dicating that transmission of the infections occurred either
anthroponotically, or that they were derived from the same
source (Molloy et al. 2010).
Since the discovery of the association between this proto-
zoan and bovine diarrhea, recognition of the zoonotic danger
of C. parvum has increased, particularly in young and HIV-
infected individuals, and higher rates of C. parvum infection
have been reported in different countries (Siwila et al. 2007;
El-Hamshary et al. 2008; Essid et al. 2008;Blancoetal.2009;
Eida et al. 2009; Adamu et al. 2010; Creek et al. 2010).
However, Morse et al. (2007) have found that the majority
of C. parvum infection cases occur in urban settings (70 %),
where animals are not found close to residences. It appears
that C. parvum is a human-adapted subtype that can also be
transmitted from person to person, and the possibility that
Environ Sci Pollut Res
infections have human origins cannot be excluded (Morse
et al. 2007). In some regions of Africa, the discovery of iden-
tical C. parvum sequences in humans, primates, and livestock
points to evidence of general Bpathogen pollution^from en-
vironmental sources (water, vegetation, and soil) in areas of
intense human/animal overlap due to anthropogenic changes
to forests (Salyer et al. 2012). Therefore, it is possible that
C. parvum can be maintained almost exclusively in humans
via geographic distinction or segregation in Africa (Molloy
et al. 2010) or via intra-specific genetic recombination (Peng
et al. 2003).
The human-adapted C. parvum GP60 subtype allelic fam-
ily IIc, which was previously named Ic, has thus far been
identified as the predominant C. parvum allele in people from
Sub-Saharan Africa, including Malawi, Nigeria, South Africa,
and Uganda, and it has never been found in animals (Leav
et al. 2002;Pengetal.2003;Akiyoshietal.2006;Akinbo
et al. 2010;Molloyetal.2010; Ayinmode et al. 2012). The
C. parvum subtype family IIm, which was discovered in
Nigeria (Molloy et al. 2010), has also never been identified
in any animal. Thus, this strain can also be considered one of
the so-called human-adapted C. parvum subtypes. Further, in
Malawi and Nigeria, the anthroponotic IIe subtype was iden-
tified (Peng et al. 2003;Akinboetal.2010,Maikaietal.2012)
in a 6-month-old diarrheic child who was solely fed breast
milk (Maikai et al. 2012).
Mixed infections of C. hominis,C. parvum, C. meleagridis,
and/or C. bovis have been previously reported (Tumwine et al.
2005; Morse et al. 2007; El-Hamshary et al. 2008;Adamu
et al. 2010;Molloyetal.2010; Ben Abda et al. 2011;
Helmy et al. 2013). The growing immune-compromised pop-
ulation in Africa has been shown to be more prone to infection
by C. meleagridis, which occurs in up to 21 % of these indi-
viduals (Morgan et al. 2000; Gatei et al. 2003; Tumwine et al.
2005; Essid et al. 2008;Blancoetal.2009; Ben Abda et al.
2011) and in 10 % of healthy people (Peng et al. 2001,Eida
et al. 2009). This high proportion of individuals infected with
C. meleagridis, compared to the small proportion of less than
1 % in the developed world, suggests that this infection is
more common on the African continent. This increased rate
of infection is attributable to environmental contamination via
shed oocysts and poor sanitation and immune suppression and
could be related to the high levels of malnutrition and HIV in
the population. These findings highlight the need to address
the epidemiologic magnitude of C. meleagridis in Africa.
Interestingly, the identification of an identical C. meleagridis
strain (AF112574) in Kenya and Tunisia (Gatei et al. 2003;
Essid et al. 2008) suggests that this strain is widespread in
Africa.
Uncommon species other than C. hominis, such as C. bovis
(Helmy et al. 2013), C. felis (Gatei et al. 2006), C. canis
(Molloy et al. 2010, Gatei et al. 2006), C. andersoni (Morse
et al. 2007), a Cryptosporidium rabbit genotype, and
C. cervine (Molloy et al. 2010), have been reported to infect
HIV-negative African children. C. serpentis was isolated from
a human in Nairobi, Kenya (Gatei et al. 2002); this is the first
report of infection of a human with this strain (Ryan et al.
2003).
The subtypes Ib, IIa, IIc, and IId are among the most com-
mon subtype families found in humans worldwide (O’connor
et al. 2011), while the common subtype families reported in
humans in many African countries include Ia, Ib, Id, and Ie
(Peng et al. 2001,2003;Leavetal.2002; Akiyoshi et al. 2006;
Mor et al. 2009; Adamu et al. 2010;Akinboetal.2010;
Ayinmode et al. 2012;Maikaietal.2012). The identical pres-
ence of the subtypes IbA13G3, IaA25R3, and IaA24R3 in
different states in Nigeria (Akinbo et al. 2010;Molloyetal.
2010, Ayinmode et al. 2012;Maikaietal.2012)are actually
unique subtypes of C. hominis. The Iii subtype (Akiyoshi et al.
2006;Molloyetal.2010) and the novel subtype family Ih
(Molloy et al. 2010) were also recovered from patients in
Uganda and Nigeria. Moreover, the zoonotic subtype groups
IIa and IId of C. parvum have been identified in different
countries (Adamu et al. 2010; Molloy et al. 2010; Helmy
et al. 2013) and have been found to be capable of causing
infection in immune-competent individuals (Helmy et al.
2013), and the C. parvum IIg and IIh alleles have also been
shown to infect immune-compromised patients (Akiyoshi
et al. 2006).
Increasing evidence indicates that the subtype affects the
disease outcome and clinical manifestations. C. hominis-in-
fected patients exhibit a longer duration of symptoms com-
pared to C. parvum-infected individuals,andtherateof
asymptomatic infection with C. hominis is higher (Houpt
et al. 2005). However, Akiyoshi et al. (2006) found that the
vast majority of children presenting with diarrhea lasting for
31 days or longer were HIV positive and were infected with
isolates belonging to the C. parvum subtype family Iii, follow-
ed by the C. hominis subtype Ie. The IIc, IIg, Ia, Ie, and Id
subtype families have been found in children with diarrhea
lasting for 21 days or less. In a South African study, children
who were less than 1-year-old exhibited particular susceptibil-
ity to C. hominis I alleles, and those that were almost 2 years
old were more prone to infection with isolates with the
C. parvum IIc genotype and presented with diarrhea for more
than 1 week (Leav et al. 2002). Definitive conclusions on this
issue, however, require further investigation, as a more de-
tailed understanding of the population structure of this ubiq-
uitous parasite is necessary.
Search strategy and selection criteria
A variety of global literature sources were used for collection of
the data, including Medline/PubMed and Google Scholar, in
addition to available electronic data from recognized
Environ Sci Pollut Res
international organizations such as the WHO and UNICEF, and
searches were performed using the terms BCryptosporidium,^
BAfrica,^BEpidemiology^and BWat e r,^BDiarrhea,^and
BDiagnosis.^All of the studies included in this review were
published in these databases between 1985 and 2013. Out of
461 studies carried out in Africa aiming to detect
Cryptosporidium infection within the population, we selected
only 100. We included only well-designed case–control,
cohort/cross-sectional studies published in English or French
and excluded any studies that were weakly designed or biased.
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