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Journal of Clinical Microbiology, March 2000, p. 1180-1183, Vol. 38, No. 3
World Health Organisation Collaborating Centre for the
Molecular Epidemiology of Parasitic Infections and State Agricultural
Biotechnology Centre, Division of Veterinary and Biomedical Sciences,
Murdoch University, Murdoch, WA 6150, Australia1; Division of Infectious
Diseases, University Hospital, CH-8091 Zurich,2
and Institute of Parasitology, University of Zurich,
CH-8057 Zurich,5 Switzerland; Division
of Parasitic Diseases, Centers for Disease Control and Prevention,
Atlanta, Georgia 303413; and Kenya
Medical Research Institute, Nairobi, Kenya4
Received 27 September 1999/Returned for modification 1 December
1999/Accepted 21 December 1999
A total of 22 Cryptosporidium isolates from human
immunodeficiency virus-infected patients from Kenya, Switzerland, and
the United States were examined at three genetic loci: the 18S
ribosomal DNA, HSP-70, and acetyl coenzyme A synthetase genes. Four
distinct Cryptosporidium genotypes were identified: (i) the
Cryptosporidium parvum "human" genotype, (ii) the
C. parvum "cattle" genotype, (iii)
Cryptosporidium felis, and (iv) Cryptosporidium
meleagridis. This is the first report of C. meleagridis in a human host. These results and those of others
indicate that immunocompromised individuals are susceptible to a wide
range of Cryptosporidium species and genotypes. Future
studies are required to understand the full public health significance
of Cryptosporidium genotypes and species in
immunocompromised hosts.
Cryptosporidium is
an important enteric pathogen that causes diarrheal illness in
humans and animals (4). In immunocompetent individuals,
infection is usually self-limiting, but in immunocompromised individuals receiving immunosuppressive drugs and human
immunodeficiency virus (HIV)-infected individuals, persistent
infections which can be life threatening may develop (3).
Cryptosporidium may account for 10 to 20% of the cases of
diarrhea in HIV-infected patients living in developed countries and as
much as 50% in underprivileged countries (12, 16). Among
HIV-infected individuals who contracted cryptosporidiosis as a result
of the infamous outbreak in Milwaukee, Wis., in 1993, the outcome of
disease was severe, with greater than 50% mortality within 6 months to
a year after the outbreak (I. Gilson, B. P. Buggy, C. F. Brunnitt, M. Busalacchi, and K. Ivantic, Int. Conf. AIDS, 1994).
The genus Cryptosporidium is a member of the phylum
Apicomplexa along with the related genera Toxoplasma,
Eimeria, and Plasmodium. To date, eight named
species of Cryptosporidium have been proposed as valid.
These include C. parvum from many mammals, C. muris from rodents and ruminants, C. felis from
cats, C. wrairi from guinea pigs, C. meleagridis
and C. baileyi from birds, C. serpentis from
reptiles, and C. nasorum from fish (4, 9).
The causative agent of cryptosporidiosis in humans and a range of
mammalian species is the species C. parvum. Recently, it has become increasingly clear, however, that C. parvum is
not a single species but is composed of a number of distinct genotypes: a "human" genotype which has so far been found only in humans; a
"cattle" genotype which is found in domestic livestock such as
cattle, sheep, and goats and which can also infect humans; a
"mouse" genotype which has been found in mice from around the world
and more recently in bats; a "pig" genotype which is found in pigs;
a "marsupial" genotype that has been found in koalas and kangaroos;
and "dog" and "ferret" genotypes which have to date been found
only in the respective hosts (7, 9, 18). Only the human
and cattle genotypes have so far been identified in immunocompetent
humans, and the public health significance of the remaining genotypes
is unknown.
The susceptibilities of immunocompromised individuals to genotypes of
C. parvum and to other species of
Cryptosporidium have not been extensively studied. The
aim of the project described here was to genetically characterize
isolates of Cryptosporidium from HIV-infected individuals in
order to determine the public health significance of genotypes of
C. parvum and other species of Cryptosporidium.
Sources of parasite isolates, diagnosis, and clinical
information.
The sources of the parasite isolates are listed in
Table 1 (see the Results section). Swiss isolates were collected
between February 1992 and July 1995; Kenyan isolates were collected
between January 1998 and January 1999. Isolates of
Cryptosporidium from the United States were collected from
1997 to 1998. Stool specimens were examined by Kinyoun carbol-fuchsin
modified acid-fast staining, and an aliquot of each positive stool was
stored either in 2.5% dichromate at 4°C or without preservatives at
DNA purification and PCR amplification of 18S rDNA and acetyl-CoA
synthetase genes.
DNA was purified as described previously
(8). The amplification conditions used to amplify a 298-bp
portion of the 18S ribosomal DNA (rDNA) gene were as described
previously (6). The primers and their sequences used to
amplify a 390-bp product from the acetyl coenzyme A (acetyl-CoA)
synthetase gene were as described previously (7). TAQ
Extender (Stratagene, La Jolla, Calif.) was included in all reaction
mixtures to minimize PCR error.
PCR amplification of the HSP-70 gene.
A two-step nested PCR
protocol was used to amplify the heat shock gene (HSP-70 gene) from
genomic DNA for nucleotide sequencing. For the primary PCR, a PCR
product of ~2,015 bp was amplified with a forward primer (5'-ATG
TCT GAA GGT CCA GCT ATT GGT ATT GA-3') and a reverse primer
(5'-TTA GTC GAC CTC TTC AAC AGT TGG-3'). The PCR mixture
consisted of 50 ng of genomic DNA, each deoxynucleoside triphosphate at
a concentration of 200 µM, 1× PCR buffer (Perkin-Elmer), 3.0 mM
MgCl2, 5.0 U of Taq polymerase (GIBCO BRL), and
40 ng of forward and reverse primers in a total reaction volume of 100 µl. Thirty-five PCR cycles (94°C for 45 s, 55°C for 45 s, 72°C for 60 s) were carried out in a Perkin-Elmer Gene Amp
PCR 9700 thermocycler with an initial hot start (94°C for 5 min) and
a final extension (72°C for 10 min). For the secondary PCR, a
fragment of ~1,950 bp was amplified by using 2.5 µl of primary PCR
product and nested forward (5'-TA/CT TCA TG/CT GTT GGT GTA TGG AGA
AA-3') and nested reverse (5'-CAA CAG TTG GAC CAT TAG ATC
C-3') primers. The PCR conditions for the secondary PCR were
identical to those for the primary PCR, except that the annealing
temperature was 45°C.
Sequencing of PCR products.
PCR products were purified by
using Qiagen spin columns (Qiagen, Hilden, Germany) and were sequenced
by using an ABI Prism Dye Terminator Cycle Sequencing kit (Applied
Biosystems, Foster City, Calif.) according to the manufacturers'
instructions. PCR products were sequenced in both directions. Sequences
were analyzed by using SeqEd, version 1.0.3 (Applied Biosystems).
Sequence analysis of the 18S rDNA gene.
The 18S rDNA gene
locus of all 22 isolates was analyzed. DNA sequence analysis at this
locus identified four distinct genotypes, with the cattle genotype
being the most common genotype identified (8 of 22) (Table
1). Six isolates were of the human
genotype. Interestingly, a total of six isolates exhibited the C. felis genotype. Three of these isolates were from Switzerland and
three were from the United States. Two isolates (isolates CZ-H78 and Ke-H392), one from Switzerland and one from Kenya, were identified as
C. meleagridis.
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Molecular Characterization of Cryptosporidium Isolates
Obtained from Human Immunodeficiency Virus-Infected Individuals Living
in Switzerland, Kenya, and the United States
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
80°C until molecular analysis. In Switzerland, sociodemographic,
clinical, and immunological data for the patients were prospectively
collected as part of the Swiss HIV Cohort Study (5), and the
patients filled in a questionnaire on risks associated with diarrhea at
the time of stool examination (16).
RESULTS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
TABLE 1.
Isolates and genotypes of Cryptosporidium used
in this study
Sequence analysis of the acetyl-CoA synthetase gene. The acetyl-CoA synthetase gene locus of 14 isolates was examined. A number of isolates, particularly those isolates which exhibited the C. felis genotype, did not produce a product with the acetyl-CoA synthetase gene-specific primers, presumably due to genetic differences between C. felis and C. parvum (H/C) at the primer binding sites. Sequence analysis of this locus identified three distinct genotypes: the cattle genotype, the human genotype, and a distinct genotype exhibited by one isolate (isolate Ke-H392) which typed as C. meleagridis at the 18S rDNA gene locus. The genotyping results for the acetyl-CoA synthetase gene locus were in agreement with those for the 18S rDNA gene locus (Table 1).
Sequence analysis of the HSP-70 gene. The HSP-70 gene locus of a smaller subset of isolates (n = 11) was analyzed. Four distinct genotypes were identified at this locus: human, cattle, C. felis, and C. meleagridis (Table 1). Genotyping results for this locus were in agreement with those for the 18S rDNA and acetyl-CoA synthetase gene loci.
Clinical information.
The majority of the clinical information
available in this study was obtained for HIV-infected patients from
Zurich, Switzerland. These patients exhibited a variety of other
concurrent AIDS-defining infections including microsporidiosis,
toxoplasmosis, and Kaposi's sarcoma (Table
2). For all patients, CD4+
lymphocyte counts were low and ranged from 0 to 110 per µl. The main
mode of HIV acquisition was via sexual contact. All patients were
experiencing chronic diarrhea that had lasted at least 4 weeks at
the time of evaluation. No concurrent infection was found in the three
C. felis-infected patients whose isolates were provided by the Centers for Disease Control and Prevention. In particular, patient US-HNO36/38 was positive twice for C. felis over a
5.5-month span and had diarrhea for the entire time.
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Numerous studies of Cryptosporidium infections in HIV-infected individuals have been conducted; however, few have genotyped the Cryptosporidium isolates from these patients in order to obtain more predictive epidemiological data as to the sources of the infections. In this study, Cryptosporidium isolates from HIV-infected individuals from Switzerland, Kenya, and the United States were analyzed at three genetic loci: the 18S rDNA, HSP-70, and acetyl-CoA synthetase gene loci. The results revealed that the majority of the patients (64%) were infected with the human and cattle C. parvum genotypes. However, a number of patients were infected with C. felis (27%) or C. meleagridis (9%). This is the first report of C. meleagridis infection in a human host.
Few genotyping studies have been conducted with isolates of Cryptosporidium from HIV-infected patients (2, 13, 15, 17). In 1998, Widmer et al. (17) conducted multilocus analysis with C. parvum isolates from HIV-infected patients. Isolates from five of the patients tested exhibited the human genotype and isolates from two patients exhibited the cattle genotype (17). No genotypic information was obtained for isolates from two subjects; the oocysts from one failed to be amplified by any of the PCR primers used, and the second isolate was amplified with only the 18S rDNA gene-specific primers (17). A possible reason for this is that the oocysts detected in these two patients were not of the human or cattle genotype. Experience in our laboratories has shown that primers that are specific for Cryptosporidium but that have been designed on the basis of the human and cattle genotypes frequently do not amplify more genetically diverse genotypes such as the pig or dog genotypes of C. parvum or other species of Cryptosporidium.
A more recent study genotyped the 18S rDNA gene locus of 10 Cryptosporidium isolates from HIV-infected individuals (13). In that study, one isolate exhibited the cattle genotype, five isolates exhibited the human genotype, three isolates exhibited the C. felis genotype, and one isolate exhibited the newly identified dog genotype (13). For some patients, multiple specimens collected over 12 months were available, and for these patients the same Cryptosporidium genotype persisted throughout the course of the patient's infection (13).
Epidemiological investigations on the mode of transmission or the possible sources of human cryptosporidial infections are difficult because there are two possible pathogenetic mechanisms of cryptosporidial disease: first, HIV-infected patients with clinically manifest cryptosporidiosis may have very recently acquired cryptosporidial infection (a new exogenous infection); and second, infection may have occurred earlier, possibly prior to the state of immunodeficiency, and the infection was activated due to the progression of the immunodeficiency (an endogenous activation of latent infection).
In the present study, three of the six patients infected with C. felis had reported having a cat as a pet. It is therefore likely that they acquired their infections from their pets. For the remaining three patients infected with C. felis, no pets were recorded. However, it is possible that these patients had been exposed to cats at some time prior to the onset of clinically apparent cryptosporidiosis. One of the patients infected with C. meleagridis reported having only a cat as a pet, but clinical information was not obtained for the second patient who was infected with C. meleagridis. C. meleagridis normally infects turkeys (4). However, this species has recently been confirmed in an Indian ring-necked parrot, which is a common aviary bird with a worldwide distribution (10). C. meleagridis may therefore have a much wider host range than was previously thought, and it is possible that these patients acquired their cryptosporidial infections via contact with aviary birds.
Recent studies have reported that among HIV-infected individuals, those with CD4+ lymphocyte counts of <100 × 106/liter are at increased risk of contracting clinical cryptosporidiosis (12, 14, 16). All the patients in the present study were suffering from chronic diarrhea, and the majority of the patients in this study had other concurrent AIDS-defining infections, such as toxoplasmosis or microsporidiosis (Table 2). The majority of patients had CD4+ lymphocyte counts which were <100 × 106/liter, and in most patients the counts were less than 50 × 106/liter. In two patients (CZ-H77 and CZ-H78), the CD4+ lymphocyte counts were 0 (Table 2). However, the small number of samples available does not allow any hypotheses regarding the different clinical courses to be made.
The majority of Cryptosporidium isolates from HIV-infected individuals from Switzerland exhibited the cattle genotype (54%). In previous studies with immunocompetent human-derived Cryptosporidium isolates from Perth, Western Australia, the human genotype was the most common genotype identified (83%; n = 36) (8). Whether there are differences in the predominance and distribution of the human and cattle genotypes between different geographic areas and whether the cattle genotype is more predominant among HIV-infected persons are issues which warrant future investigation.
Six of the isolates examined in this study were from Kenya; four of
these were of the human genotype, and the remaining two (isolates
Ke-H271 and Ke-H392) were of the cattle genotype and C. meleagridis, respectively. Little is known about the prevalence of
Cryptosporidium in African countries, and this is the
first time that Cryptosporidium isolates from Kenyan
HIV-infected patients have been analyzed genetically. Recent research,
however, indicates that the prevalence of Cryptosporidium in
African HIV-infected patients may be high. A prospective
cross-sectional study of 75 consecutive HIV-seropositive adult
patients admitted to a government hospital in Nairobi, Kenya, revealed
that Cryptosporidium was the most common pathogen (17%).
Thirty-one (41%) patients died, and detection of
Cryptosporidium oocysts was the single most significant predictor of death (
2 = 5.2; P <0.05)
(11). These results are in agreement with those of an
earlier study performed in Nairobi, Kenya (1). The study reported that Shigella flexneri, Salmonella
enterica serovar Typhimurium, and C. parvum were the
most common fecal pathogens among HIV-infected and non-HIV-infected
individuals studied (1).
In conclusion, the results of the present study and those of other studies indicate that immunocompromised individuals are susceptible to a wide range of Cryptosporidium species and genotypes and that host factors must play a role in controlling susceptibility to these divergent parasites. Future studies with larger numbers of AIDS patients for whom more extensive clinical information is available are required in order to understand the full public health significance of Cryptosporidium species and genotypes in immunocompromised hosts.
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ACKNOWLEDGMENTS |
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We thank Anne Morse, Jeff Inungu, and S. K. Kang'ethe for assistance.
This research was supported by the Public Health Research and Development Committee of the National Health and Medical Research Council of Australia and the Centers for Disease Control and Prevention Opportunistic Infections Fund.
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FOOTNOTES |
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* Corresponding author. Mailing address: Murdoch University, Murdoch, WA 6150, Australia. Phone: (08) 9360 2457. Fax: (08) 9310 4144. E-mail: morgan{at}numbat.murdoch.edu.au.
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Discussion
References
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Journal of Clinical Microbiology, March 2000, p. 1180-1183, Vol. 38, No. 3
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