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Am. J. Trop. Med. Hyg., 73(5), 2005, pp. 921-925
Copyright © 2005 by The American Society of Tropical Medicine and Hygiene

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CRYPTOSPORIDIOSIS AND MICROSPORIDIOSIS IN UGANDAN CHILDREN WITH PERSISTENT DIARRHEA WITH AND WITHOUT CONCURRENT INFECTION WITH THE HUMAN IMMUNODEFICIENCY VIRUS

JAMES K. TUMWINE, ADDY KEKITIINWA, SABRINA BAKEERA-KITAKA, GRACE NDEEZI, ROBERT DOWNING, XIAOCHUAN FENG, DONNA E. AKIYOSHI, AND SAUL TZIPORI*
Department of Paediatrics and Child Health, Mulago Hospital, Makerere University Medical School, Kampala, Uganda; Uganda Virus Research Institute, Entebbe, Uganda; Division of Infectious Diseases, Tufts Cummings School of Veterinary Medicine, North Grafton, Massachusetts


ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Cryptosporidium spp. and Enterocytozoon bieneusi are enteric pathogens that have emerged as significant causes of persistent diarrhea (PD) in immunologically compromised individuals particularly in association with HIV/AIDS. We conducted a cross-sectional study on the clinical epidemiology of E. bieneusi and Cryptosporidium in children with PD, with and without HIV/AIDS, attending Uganda’s Mulago National Referral Hospital. Two hundred forty-three children aged < 60 months, admitted between November 2002 and May 2003 with PD (> 14 days), were analyzed for HIV status and CD4 lymphocyte counts, and stools were screened for the presence of E. bieneusi and Cryptosporidium by microscopy and positive samples genotyped by polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) analysis. Eighty (32.9%) of the children were excreting E. bieneusi, and 76 (31.3%) were excreting Cryptosporidium. Ninety-one of the 243 children had HIV, of who 70 (76.9%) had E. bieneusi, versus 10 (6.6%) of the 152 without (odds ratio = 47.33; 95% CI = 19.88 to 115.97), while 67 (73.6%) had Cryptosporidium, versus 9 (5.9%) without (odds ratio = 44.36; 95% CI = 18.39 to 110.40). Children with counts < 25% CD4 cells were more likely to have either E. bieneusi (odds ratio = 7.42; 95% CI = 3.77 to 14.69) or Cryptosporidium (odds ratio = 6.45; 95% CI = 3.28 to 12.76) than those with higher CD4 percentages. However, only HIV status was independently associated with either Cryptosporidium or E. bieneusi. Among the 243 children with PD, 67 (27.8%) were infected with both enteric pathogens, with HIV being the only independent predictor of coinfection. Finally, some 81% of HIV-infected children with PD excreted one or both organisms, compared with only 10% of children with PD testing negative for HIV. Seventy-four percent of isolates were C. hominis, the anthroponotic species, 17% were C. parvum, the zoonotic species, and 8% were a mixture of the two or others.


INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Cryptosporidiosis and microsporidiosis are two enteric microorganisms most commonly associated with persistent diarrhea (PD) and wasting in immunologically compromised individuals involving mostly people with HIV/AIDS, and against which there is no effective therapy.1–4 Whereas cryptosporidiosis is known to also be a common serious cause of acute diarrhea in all ages of immunologically healthy people,5,6 microsporidiosis, as judged by the lack of scientific documentation, does not appear to be associated with neither acute illness, nor, it seems in general, with immunologically healthy people. Indeed, Enterocytozoon bieneusi, the microsporidia most commonly associated with PD and wasting in people with HIV/AIDS, was unknown prior to the emergence of AIDS in the mid-1980s.7 Until the introduction of antiretroviral therapy (ART) in 1995–1996,3 both were serious opportunistic infections that complicated HIV/AIDS in developed countries. In the absence of ART, adults in developing countries, unfortunately, continue to suffer the consequences of cryptosporidiosis and microsporidiosis of profound PD and wasting in patients with HIV/AIDS.1–3,8–10 Although there are several reports from Africa on cryptosporidiosis in children,1,11–16 there is little on microsporidiosis. Furthermore, most of the worldwide reports, with a few exceptions,17,18 tend to focus on adults with HIV/AIDS.19–21

In previous communications, we have shown that cryptosporidiosis22 and microsporidiosis23 are very common infections in infants and children in Uganda aged < 60 months. In these studies, while cryptosporidiosis was shown to be closely linked with acute or persistent diarrhea wasting and poor prognosis in some 25% of 1,779 children investigated, there was no evidence that E. bieneusi, observed in approximately 17% in the same population, was clearly associated with illness.23 The role of HIV/AIDS in these children however was not determined, which may explain the lack of apparent clinical significance of E. bieneusi in the overall study population of some 1,779 children.23 Consequently, an additional study was undertaken to specifically determine the contribution of cryptosporidiosis and microsporidiosis to pediatric PD, with and without HIV/AIDS.


MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study design, site, and population. Children aged less than 60 months, admitted to Mulago Hospital with PD (> 14 days) and whose caretakers consented to participate in the study, were recruited from November to 2002 to May 2003 (Table 1Go). None of the patients were on ART on recruitment. Children with measles, dysentery, or cancer were excluded from the study.


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TABLE 1
Features of children with persistent diarrhea by HIV status
 
This was a cross-sectional study in which we determined the prevalence, by HIV status, of E. bieneusi and Cryptosporidium among children attending Mulago Hospital with PD. The study was carried out in the pediatric diarrhea treatment ward of Mulago Hospital, in Kampala. Mulago Hospital is the largest referral and teaching hospital in the country. On average, 40 to 60 patients are admitted each day, of these, at least 5 have PD. Patients aged less than 60 months are admitted to the diarrhea treatment ward. After explaining the purpose of the study to the parents/caretakers and getting informed consent, patients fulfilling inclusion criteria were enrolled into the study consecutively until the sample size was reached.

Stools were collected from the diapers or obtained directly and placed into plastic containers, using disposable gloves. The stools were taken daily to the Joint Clinical Research Center (JCRC) in Kampala, for storage at 4°C, after which they were shipped unfrozen in batches to Tufts University, North Grafton, MA. The stools were tested for E. bieneusi by PCR,23 and for Cryptosporidium by immunofluorescence microscopy using specific C. parvum antibodies,2 and subsequently confirmed and genotyped by polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) analysis.22 HIV tests and CD4+ lymphocyte counts were carried out at the Uganda Virus Research Institute. Blood was transported at ambient temperature and CD4 cell counts were performed within 12 hours. The CD4+ lymphocyte count was done using dual color flow cytometry (FACScan instrument and MultiSet software, Becton Dickinson, Franklin Lakes, NJ). The HIV status was determined using two enzyme linked immunoassays (Recombigen HIV-2, Trinity Biotech plc, Bray CC, Wicklow, Ireland; and Wellcozyme HIV Recombinant, Murex Biotech Ltd., Dartford, UK), and Western blots as well where necessary. For children aged below 18 months who had a positive HIV test by ELISA, their status was confirmed by reverse transcriptase PCR.

Sample size and statistical tests. To estimate the prevalence of E. bieneusi, a sample size of 211 children was calculated using a formula by Kish and Leslie.24 This was based on an estimated prevalence of 18.8% of E. bieneusi among a population of 2,140 children seen in the clinic over a period of 7 months, and allowing for a 5% error and 95% confidence intervals (CI).

Data were entered into EPIINFO version 6 (Centers for Disease Control and Prevention, Atlanta, GA) and analyzed using SPSS. Statistical significance differences between CD4 cell counts by E. bieneusi or Cryptosporidium status were determined using Mann-Whitney U nonparametric tests. For normally distributed data, the Student t test was used to compare differences in mean values. Categorical variables were compared using the {chi}2 test or Fisher exact test where the number in any cell was five or less; with the corresponding odds ratios, 95% confidence intervals and P values. A P value of less than 0.05 was considered significant. Logistic regression analysis was used to establish factors independently associated with coinfection of the two organisms.

Ethical issues. The study was reviewed and approved by the Makerere University Medical School and Mulago Hospital Research and Ethics Committee. All interviews were conducted in the local language (usually Luganda or English, which are widely spoken) with a translator, where necessary, and consent forms were translated into the relevant local language and the study physician obtained informed consent. Parents or guardians were offered pre- and post-HIV counseling; and relevant treatment was offered to the children and the results were given to the attending physician as soon as they were available. Children testing positive for HIV were referred to the Mulago Hospital Pediatric Infectious Disease Clinic for follow up and further management.


RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Two hundred forty-three children with PD were recruited, of who 145 (59%) were males, with an age range of 1–60 months (mean = 13.0; SD = 8.67). Overall, 80 (32.9%) of the 243 children with PD were excreting E. bieneusi in the stool, and 76 (31.3%) were excreting Cryptosporidium oocysts. In contrast, in previous studies the rate of excretion of Cryptosporidium oocysts among 667 healthy children was 8.5%22 and of E. bieneusi spores 16.8%.23 Table 1Go shows that the HIV status of these children had little impact on the degree of malnutrition, as all children were selected on the basis of being hospitalized with PD and or chronically malnourished.

Prevalence of E. bieneusi by HIV status. Children with HIV infection were more likely to have E. bieneusi in their stool than HIV negative children. Of the 91 HIV-positive children, 70 (76.9%) were excreting E. bieneusi, compared with only 10 (6.6%) of the 152 without HIV (odds ratio = 47.33; 95% CI = 19.88 to 115.97; P < 0.0001). Children with CD4 lymphocyte counts below 25% were more likely to excrete E. bieneusi than those with higher percentage (24% versus 9%; odds ratio = 7.42; 95% CI = 3.77 to 14.69; P = 0.002). Overall, children with E. bieneusi were more likely to be older and have a lower percentage of CD4 cells than children free of the infection. Among the clinical features, only HIV status was significantly associated with E. bieneusi (Table 2Go).


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TABLE 2
Clinical features of children by Enterocytozoon bieneusi status
 
Prevalence of Cryptosporidium by HIV status. Overall, 76 (31.3%) of the 243 children with PD were excreting Cryptosporidium oocysts in the stool. Children with HIV were more likely to have Cryptosporidium oocysts than children without. Of the 91 children with HIV, 67 (73.6%) had Cryptosporidium, compared with only 9 (5.9%) of the 152 children without (odds ratio = 44.36; 95% CI = 18.39 to 110.40; P < 0.0001). Children with low CD4 cell percentages (< 25%) were more likely to have Cryptosporidium than those with higher percentages (odds ratio = 6.45; 95% CI = 3.28 to 12.76; P < 0.0001). Clinical features of children excreting Cryptosporidium oocysts are shown in Table 3Go. Only HIV infection was independently associated with Cryptosporidium.


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TABLE 3
Clinical features of children by Cryptosporidium status
 
Genotypic analysis of the Cryptosporidium DNA on 76 children showed that 56 (73.7%) were the anthroponotic C. hominis (or Type 1), 14 (18.4%) were the zoonotic C. parvum (or Type 2), 3 (3.9%) were a mixture of both, and 3 (3.9%) were C. meleagridis, the avian species. Although the numbers were too small for a firm conclusion, C. parvum was significantly more prevalent among children with HIV than C. hominis (odds ratio = 0.167; 95% CI = 0.036 to 0.771; P = 0.014), and was more likely to occur together with E. bieneusi (P = 0.03; Fisher exact test), indicating a possible common source of infection.

Co-infection with E. bieneusi and Cryptosporidium. Of the 243 children, 67 (27.8%) were excreting both E. bieneusi and Cryptosporidium in their stool. This means that 67 (83.8%) of the 80 children with E. bieneusi had Cryptosporidium; and 67 (88.2%) of the 76 children with Cryptosporidium had E. bieneusi. Factors associated with coinfection are shown in Table 4Go. However only infection with HIV was independently associated with coinfection.


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TABLE 4
Factors associated with coinfection with E. bieneusi and Cryptosporidium among children with persistent diarrhea
 
One or both microorganisms were present in the stool of 89 (36.6%) of the 243 PD children recruited for this study, and in 74 (81.3%) of the 91 children with HIV, compared with 15 of 152 (9.9%) children without.

Severe dehydration. Although only 18 (7.4%) of the 243 children with PD had severe dehydration, the case fatality rate was high (35.7%), compared with only 12.8% among children who were not severely dehydrated. Factors associated with severe dehydration included E. bieneusi, oral thrush and others as shown in Table 5Go. After regression analysis, only oral thrush was independently associated with severe dehydration.


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TABLE 5
Factors associated with severe dehydration among children with persistent diarrhea
 

DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
There have been several studies on cryptosporidiosis from Africa.8–16 These early studies focused either on adults with AIDS, or on children but with no specific reference to their HIV/AIDS and immune status, or to the nature of the parasites they harbored. Recently used sophisticated molecular epidemiologic techniques have increased the sensitivity of detection, as well as allowing for a simultaneous genetic characterization of the pathogens isolates obtained from patients. There are no publications from Africa, or from anywhere else, addressing the epidemiology, natural history, and the clinical significance of microsporidiosis in children with HIV/AIDS. There are a few that report E. bieneusi infections in African adults with HIV/AIDS.1,2,21 To an extent, this publication fills some of these gaps.

In this study we determined the prevalence of both E. bieneusi and Cryptosporidium among children with PD (lasting > 14 days), in whom their HIV and immune status (CD4 cell count) were determined. Whereas similar information had been previously reported in a few studies of adult patients with HIV,2,3 our series appears to be the largest record of African children infected with HIV and PD who were excreting E. bieneusi and Cryptosporidium. That E. bieneusi and Cryptosporidium were found in children with PD was not surprising and is consistent with previous observations in this22,23 and in other populations.1,11,17 What was astonishing is the very high percentage of HIV-infected children with PD who were excreting either Cryptosporidium (73.6%), E. bieneusi (76.9%), both (69.2%), or one or both (81.3%). In contrast, only 8.5% of 1,779 children without diarrhea, sampled at Mulago Hospital, were excreting Cryptosporidium, regardless of HIV or immune status.22 This is higher than in any other recorded HIV population, including adults. This may be, as stated earlier, due to the sensitivity of the genetic methods used in these studies, rather than an exceptionally high prevalence in these children. These observations indicate that these two pathogens alone may in fact be responsible for the great majority of PD in African children with HIV/AIDS. As in our previous study on E. bieneusi,23 there was no significant association between infection in this subpopulation and malnutrition even after controlling for HIV status and CD4 counts/percentages.

Children with E. bieneusi or Cryptosporidium had more advanced HIV disease, as shown by lower CD4 cell counts and percentages, further confirming the view that these pathogens seem to be markers of advanced AIDS.25 The outcome was unfavorable for those with severe dehydration and low CD4 cell counts. There are limited observations on coinfection from sub Saharan Africa. In the current study the risk factors for the coinfection were infection with HIV, low CD4 cell percentages, and generalized lymphadenopathy. This implies that HIV-positive children who have PD need to be tested for both of these opportunistic enteric infections.

Consistent with our earlier observations,22 the ratio between the prevalence of C. hominis, the anthroponotic species (74%), and C. parvum, the zoonotic species (18%), was maintained, indicating that this ratio is a stable phenomenon. This is significant and indicates that infection is acquired directly from human contact, or indirectly through drinking water contaminated with human effluent. This is because C. hominis, unlike C. parvum, predominantly perpetuates in humans. The limited data that C. parvum occurred at higher frequency in children with HIV may have clinical and epidemiologic implications. One plausible explanation for the higher frequency of C. parvum infections in children with HIV is that these children are probably exposed to cryptosporidiosis multiple times and once they are exposed to C. parvum, it predominates thereafter. This is based on our previous work in which C. parvum was shown to predominant over C. hominis in an infected host.26 Observations that C. parvum was also found more frequently with E. bieneusi than was C. hominis may point to a possible common source of infection. Both of these observations, however, need to be further investigated with a larger number of children. It is important to identify the major sources of these pathogens, through community based epidemiologic studies, with a view to formulate appropriate control measures.

Although nitazoxanide and fumagillin are drugs that have been used to treat cryptosporidiosis and microsporidiosis, respectively, neither is effective in eradicating these chronic infections in HIV-infected individuals and consequently are not commonly used for such patients. In addition, nitazoxanide is not yet FDA-approved for use in immunocompromised individuals,27 and fumagillin is considered toxic for children.28 As experience with ART in African children with HIV is limited, the impact of this treatment on cryptosporidiosis and microsporidiosis in these children who are often mal-nourished is also unknown. Monitoring the impact of ART on these pathogens will hopefully be the next step.

Although there are several rapid staining methods used for the diagnosis of microsporidia spores in stool specimens,28 they are nonspecific for E. bieneusi, the microsporidia we had targeted for these studies, as distinct from others including Encephalitozoon intestinalis. In contrast, the molecular genetic tools we have used, while laborious and not commonly used in routine clinical diagnosis, provided superior specificity and sensitivity. The PCR technique that has been in practice in this laboratory for a decade has, in addition to greater specificity and sensitivity, the major advantage of detecting both pathogens simultaneously, including genotyping in the case of cryptosporidiosis and sequence analysis of E. bieneusi.

Conclusion. E. bieneusi and Cryptosporidium are highly prevalent in Ugandan children, especially those immunocompromised by HIV/AIDS. Coinfection with both organisms occurs in 81% of those with HIV/AIDS. There is a need to introduce ART in these children to control HIV and indirectly PD that is associated with these two enteric infections.

Received December 20, 2004. Accepted for publication June 14, 2005.

Acknowledgments: The authors thank Dr. Shihab, nurses, doctors, and Albert Maganda for data handling; Peter Mugyenyi, Cissy Kityo, S. Tugume, and staff of the Joint Clinical Research Centre and the Uganda Virus Research Institute for support with lab work. We also thank Julia Dilo for the PCR analyses.

Financial support: This work was supported by NIH awards NO-AI-25466, RO1 AI-50471, and R21 AI-52792.

* Address correspondence to Saul Tzipori, Division of Infectious Diseases, Tufts Cummings School of Veterinary Medicine, 200 Westborough Road, North Grafton, MA 01536. E-mail: saul.tzipori{at}tufts.edu Back

Authors’ addresses: James K. Tumwine, Addy Kekitiinwa, Sabrina Bakeera-Kitaka, Grace Ndeezi, and Robert Downing, Department of Paediatrics and Child Health, Mulago Hospital, Makeere University Medical School, Kampala, Uganda. Xiaochuan Feng, Donna E. Akiyoshi, and Saul Tzipori, Division of Infectious Diseases, Tufts Cummings School of Veterinary Medicine, 200 Westboro Road, North Grafton, MA 01536, E-mail: saul.tzipori{at}tufts.edu.

Reprint requests: Saul Tzipori, Division of Infectious Diseases, Tufts Cummings School of Veterinary Medicine, 200 Westborough Road, North Grafton, MA 01536, Telephone: 508-839-7955, Fax: 508-839-7977, E-mail: saul.tzipori{at}tufts.edu.


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 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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A. Espern, F. Morio, M. Miegeville, H. Illa, M. Abdoulaye, V. Meyssonnier, E. Adehossi, A. Lejeune, P. D. Cam, B. Besse, et al.
Molecular Study of Microsporidiosis Due to Enterocytozoon bieneusi and Encephalitozoon intestinalis among Human Immunodeficiency Virus-Infected Patients from Two Geographical Areas: Niamey, Niger, and Hanoi, Vietnam
J. Clin. Microbiol., September 1, 2007; 45(9): 2999 - 3002.
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 J. Clin. Microbiol.Home page
S. S. R. Ajjampur, B. P. Gladstone, D. Selvapandian, J. P. Muliyil, H. Ward, and G. Kang
Molecular and Spatial Epidemiology of Cryptosporidiosis in Children in a Semiurban Community in South India
J. Clin. Microbiol., March 1, 2007; 45(3): 915 - 920.
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 J DAIRY SCIHome page
S. R. Starkey, K. R. Kimber, S. E. Wade, S. L. Schaaf, M. E. White, and H. O. Mohammed
Risk factors associated with Cryptosporidium infection on dairy farms in a New York State watershed.
J Dairy Sci, November 1, 2006; 89(11): 4229 - 4236.
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 J Med MicrobiolHome page
S. E. Stroup, S. Roy, J. Mchele, V. Maro, S. Ntabaguzi, A. Siddique, G. Kang, R. L. Guerrant, B. D. Kirkpatrick, R. Fayer, et al.
Real-time PCR detection and speciation of Cryptosporidium infection using Scorpion probes.
J. Med. Microbiol., September 1, 2006; 55(Pt 9): 1217 - 1222.
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 Infect. Immun.Home page
X. Feng, D. E. Akiyoshi, A. Sheoran, I. Singh, J. Hanawalt, Q. Zhang, G. Widmer, and S. Tzipori
Serial Propagation of the Microsporidian Enterocytozoon bieneusi of Human Origin in Immunocompromised Rodents.
Infect. Immun., August 1, 2006; 74(8): 4424 - 4429.
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 Am J Trop Med HygHome page
W. GATEI, C. N. WAMAE, C. MBAE, A. WARURU, E. MULINGE, T. WAITHERA, S. M. GATIKA, S. K. KAMWATI, G. REVATHI, and C. A. HART
Cryptosporidiosis: prevalence, genotype analysis, and symptoms associated with infections in children in kenya.
Am J Trop Med Hyg, July 1, 2006; 75(1): 78 - 82.
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