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| Year : 2012 | Volume
: 23
| Issue : 4 | Page : 677-683 |
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| Intestinal fungal and parasitic infections in kidney transplant recipients: A multi-center study |
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Afsoon Emami Naeini1, Mehran Sharifi1, Shahrzad Shahidi1, Shahram Taheri1, Shiva Seirafian1, Dyana Taheri2, Mahdi Tazhibi3, Sayyed Hosein Hejazi4, Pardis Emami Naini1, Asghar Amini Harandi5
1 Department of Nephrology, Isfahan Kidney Diseases Research Center, Isfahan University of Medical Science, Isfahan, Iran
2 Department of Pathology, Isfahan Kidney Diseases Research Center, Isfahan University of Medical Science, Isfahan, Iran
3 Department of Statistics, Isfahan Kidney Diseases Research Center, Isfahan University of Medical Science, Isfahan, Iran
4 Department of Parasitology and Mycology, Isfahan Kidney Diseases Research Center, Isfahan University of Medical Science, Isfahan, Iran
5 JahromUniversity of Medical Science, Jahrom, Iran
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| Date of Web Publication | 9-Jul-2012 |
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 Abstract | | |
Kidney transplant recipients are susceptible to various infections due to the use of immunosuppressive drugs. The present study was performed as studies on the prevalence of intestinal fungal and parasitic infections in kidney transplant recipients are limited. A total of 150 kidney transplant recipients and 225 matched immunocompetent outpatients, who were referred to the laboratory of Noor Hospital, Isfahan, were studied. After recording demographic characteristics, direct test and specific laboratory cultures were carried out on the stool specimens. Patients were instructed on sanitary rules and, during each medical visit, they were reminded of the same. The overall prevalence of intestinal parasitic and fungal infections was 33.3% and 58.7%, respectively, in transplant recipients and 20% and 51%, respectively, in the control group; the difference was not statistically significant. The most prevalent intestinal parasite was Entameba coli, which was seen in 9.3% of the study patients and 6.7% of the controls. The most prevalent fungus was Candida sp., which was seen in 22% of the study patients and 24.4% of the control group. Coexisting infection with two or more fungi was seen in 14.8% and 3.4% in the case and control groups, respectively; P <0.001. Interestingly, there was no significant difference in the prevalence of infection by a single organism between the two groups. However, co-existing infection with two or more species was more prevalent in transplant recipients. We conclude that further investigations are needed to evaluate the pathogenesis of infection with these microorganisms.
How to cite this article:
Naeini AE, Sharifi M, Shahidi S, Taheri S, Seirafian S, Taheri D, Tazhibi M, Hejazi SH, Naini PE, Harandi AA. Intestinal fungal and parasitic infections in kidney transplant recipients: A multi-center study. Saudi J Kidney Dis Transpl 2012;23:677-83 |
How to cite this URL:
Naeini AE, Sharifi M, Shahidi S, Taheri S, Seirafian S, Taheri D, Tazhibi M, Hejazi SH, Naini PE, Harandi AA. Intestinal fungal and parasitic infections in kidney transplant recipients: A multi-center study. Saudi J Kidney Dis Transpl [serial online] 2012 [cited 2013 May 21];23:677-83. Available from: http://www.sjkdt.org/text.asp?2012/23/4/677/98110 |
| Introduction | |  |
Parasitic and fungal infections, especially the opportunistic ones, are one of the major problems in immunocompromised patients. [1] Kidney transplant recipients comprise a group of immunocompromised patients who are susceptible to various infections. [2],[3],[4] Considering the paucity of studies carried out to determine the prevalence of parasitic and fungal infections in Iranian kidney transplant recipients, we designed this study to determine the prevalence of intestinal fungal and parasitic infections in a group of kidney transplant recipients in Iran.
| Materials and Methods | | |
This is a descriptive-analytical, cross-sectional study that evaluated 150 kidney transplant recipients taking immunosuppressive drugs (cyclosporine, prednisolone, azathioprine or mycophenolate mofetil). The cases were randomly selected from the Noor Hospital Laboratory, Isfahan, Iran. The control group consisted of 225 outpatients randomly selected from among patients who were referred to the Noor Hospital Laboratory. Inclusion criteria for the control group included negative history of taking immunosuppressive drugs such as corticosteroids, cyclophosphamide, cyclosporine, azathioprine, cellcept, chlorambucil and chemotherapy drugs, and negative history of immunosuppressive diseases such as malignancies, acquired immune deficiency syndrome (AIDS), congenital immunologic diseases, chronic renal failure and hepatic failure. Sequential sampling method was used to select the participants. Demographic data of all participants were recorded, including gender, age, level of education (illiterate, below high school diploma, high school diploma or higher), general hygiene condition (good, fair or poor according to clothing and skin hygiene), [5] living place (urban or rural) and keeping pets at home or workplace. In addition, the patients' gastrointestinal complaints such as constipation and diarrhea were recorded. Student's t-test was used to compare the age between the two groups. Comparison of age and relative frequency of parasitic and fungal infections was carried out using Chi-square test.
Stool specimens of all participants were sent to the same research laboratory of mycology and parasitology soon after collection. The following parasitological tests were conducted on all the stool samples: direct wet mount with normal saline solution, direct wet mount with lugol solution, formalin-ether concentration, modification of Sheater's sugar floatation, modified Zeil-Neilson's staining and Harada-Mori's tube method culture. To identify the fungal species, stool samples were cultured in SC medium (Sabouraud's dextrose agar medium containing chloramphenicol). After 48-h of incubation at room temperature, cultures were studied for their morphological properties (fungal colony color and shape). To verify the isolated types, Giemsa and Gram staining were done. Additionally, to evaluate the presence of Cryptococcus neoformans, Sudan black dye staining was performed.
| Results | | |
The mean and standard deviation (mean ± SD) of age were 41.9 ± 8.1 and 39.1 ± 6.2 years, in the case and control groups, respectively (P >0.05). About 69.4% of the case group (104 patients) and 52.2% of the control group (118 patients) were male.
In the transplant recipients, the mean duration post-transplant when this study was conducted was 43 ± 8.2 months, and all had been taking immunosuppressive drugs since the date of transplantation. Among transplant recipients, 50 (33.3%) were infected by one or more intestinal parasites and 88 (58.7%) were infected by one or more intestinal fungi. Among the control group, these mixed infections were seen in 45 (20%) and 115 cases (51.1%), respectively. The Chi-square test did not identify any significant difference between the two groups in this regard.
The prevalence of intestinal protozoa in the participants of the study is shown in [Table 1]. Entameba coli was the most prevalent protozoan, with a prevalence of 9.3% and 6.7% in the case and control groups, respectively. The second most prevalent protozoan was Endolimax nana, with a prevalence of 8% and 6.2% in the case and control groups, respectively. | Table 1: Prevalence of intestinal protozoa in the kidney transplant recipients and control groups.
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Only one of the transplant recipients was infected by Ascaris lumbercoides, and two patients in the control group were infected by Hymenolepis nana.
Among the kidney transplant recipients with parasitic infections, 90% were infected by one type, 8% with two types and 2% with three types. In the control group, 86.7% were infected by one type, 2.3% by two types and 6.7% were infected by three types of parasites. The two groups were significantly different regarding the prevalence of parasitic infection with one, two or three types of parasites (P <0.001).
The prevalence of intestinal fungi in the two groups is shown in [Table 2]. Candida sp. was the most prevalent fungus in both the transplant recipient and control groups (22% and 24.4%, respectively). The second most prevalent fungus was the Mucor sp., with a prevalence of 11.3% and 12% in the transplant recipient and control groups, respectively. | Table 2: Prevalence of intestinal fungi in the kidney transplant recipients and control groups.
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Overall, 85.2%, 12.5% and 2.3% of the transplant recipients were infected by one, two and three types of intestinal fungi, respectively; while 96.6% and 3.4% of the control group were infected by one and two types of intestinal fungi, respectively. The two groups were significantly different concerning co-infection with multiple types of intestinal fungi (P <0.001).
No significant relationship was observed between the prevalence of fungal and parasitic infections and gender, level of education, age, location of dwelling and keeping pets at home or workplace. The participants were categorized into three groups regarding general hygienic condition: good (clean skin and clothes), moderate (fairly dirty and scaling skin and rather dirty or soiled clothes) and poor (dirty and scaling skin and very dirty and soiled clothes). The prevalence of parasitic and fungal infections was not significantly correlated with the general hygiene condition [Table 3]. | Table 3: Prevalence of intestinal fungi and parasites in the kidney transplant recipient and the control groups and their correlation with the demographic and studied variables.
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| Discussion | | |
In the present study, the prevalence of parasitic and fungal infections was higher in kidney transplant recipients (58.7% and 33.3%, respectively) compared with the control group (20% and 51.1%, respectively). Although the difference is not statistically significant, it indicates the high prevalence of fungal and parasitic infections in immunocompromised patients. Also, the prevalence of parasitic infection with one, two and three types of parasites was higher in the immunocompromised patients rather than in the control group. The findings are of great importance considering the increase in patients with cancer and the increasing rate of organ transplantation, both of which require the administration of immunosuppressive drugs. Despite various reports on fungal and parasitic infections in immunocompromised patients, [6],[7],[8],[9],[10],[11] most of these studies, local or worldwide, were limited to a special type of fungus or parasite or a specific age group, and most were carried out on HIV-infected patients. [6],[10]
Parasite infections
The prevalence of Entameba coli in transplant recipients and control groups was 9.3% and 6.7%, respectively; this was the most common parasite isolated. In a study carried out by Athari et al on kidney transplant recipients and cancer patients, the most common intestinal parasite was found to be Blastocystis huminis. The prevalence of infection with the parasite was 18.2% in these immunocompromised patients (385 cancer patients and kidney transplant recipients). [12] Other studies on immunocompromised patients have reported Blastocystis huminis (14.9%), [13] Giardia lambelia (7.3%) [14] and Isospora belli (26.8%), [15] as the most common intestinal infectious pathogens.
The high prevalence of Entameba coli and Endolimax nana indicates the important role of these parasites in intestinal infections. Various studies have reported the prevalence of these parasites to be 7.3% [15] and 3.8% [9],[10] in kidney transplant recipients and cancer patients, respectively.
The prevalence of infection with Giardia lamblia in the general population was 7.3% and 3.8% [9],[10] in immunocompromised patients. [14] Cryptosporidium infection was detected in just one case in the present study, while its reported prevalence in various studies worldwide ranges from 0% to 30%. [16] Memar et al studied 781 patients with HIV/ AIDS and 1220 non-HIV infected individuals; they found a prevalence of Strongyloides stercoralis of 0.26% (two persons) in HIV-infected patients in comparison with 0.33% (four persons) in the control group. Furthermore, the prevalence of Hymenolepis nana was 0.13% (one person) in HIV-infected patients compared with 0.16% (two persons) in the control group. [14] Another study carried out on 78 HIV-infected patients and 26 normal persons in Ethiopia reported the prevalence of Ascaris lumbericoides to be 30.8% (24 persons) in the HIV-infected group versus 23.1% (six persons) in the control group. [9] In addition, the study performed by Zali et al reported infection with Hymenolepis nana in two HIV-infected patients (0.9%). [15] In our study, one case of Ascaris lumbercoides infection and two cases of Hymenolepsis nana infection were diagnosed, while no cases of Strongyloides stercoralis infection were seen. Generally, the prevalence rate of infection with nematodes is much lower than parasitic infection in kidney transplant recipients and those who take immunosuppressive drugs. [12] This finding has been observed in other investigations as well. However, the importance of Strongyloides stercoralis infection is known in kidney transplant recipients and immunocompromised patients as the infection in these patients presents as disseminated strongyloidiasis and causes death. Fortunately, by employing advanced laboratory techniques, no Strongyloides stercoralis infection was found in the present study.
Fungal infections
The prevalence of infection with Candida sp in our study was 22% and 24.4% in the case and control groups, respectively, and was the most prevalent intestinal fungal infection. Rezaeian et al also reported Candida sp. infection as the most common fungal infection in HIV-infected patients. [8] The second most common fungal infection was reported to be that with Mucor sp. In a study conducted in Sudan to determine the prevalence of opportunistic mycelial fungi in 53 transplant recipient patients, the prevalence of Mucor sp., Rhizopus sp., Fusarium sp. and Aspergillus sp. was reported to be 1.8%, 3.8%, 3.8% and 69.8%, respectively. [7] Immaculata et al found that 2.43% of the patients in an Indian tertiary care hospital had infection with Aspergillus sp. [17] In our study, the prevalence of infection with Aspergillus sp. was 1.3% and 0.4% in the kidney transplant recipients and control groups, respectively. Fungal infections such as Aspergillus sp. infections are common nosocomial infections, threatening the life of patients in oncology, critical care and organ transplantation wards. Yehia et al reported three cases of Phaeohyphomycosis infections in kidney transplant recipients. They also found two cases of subcutaneous Alternaria infections and one case infected by subcutaneous Phyalofora fungus. [18] Moreover, another study carried out in Philadelphia by Singh et al. reported one case of esophageal infection by Cladophialophora bantiana in a kidney transplant recipient. [11] The current study detected only one case of mycelial fungus infection, i.e. with Nigrosporon. Although Cryptococcus neoformans and Histoplasma capsulatum are considered to be the pathogens responsible for gastroenteritis in immunocompromised patients, [8] these organisms were not isolated in our study.
In the present study, no significant correlation was observed between the prevalence of intestinal parasitic and fungal infections and level of education, living place, keeping pets at home or workplace and general hygienic condition. All patients were instructed to follow sanitary rules without fail; this was done initially and during each visit. The rules included correct method of washing hands, fruits and vegetables, avoiding consumption of contaminated water and food and avoiding use of readymade foods.
The studies carried out in different countries to determine the parasitic and fungal infections in kidney transplant recipients are limited. Besides, most studies performed on immunocompromised patients did not consider the role of different variables. It seems that the occasional differences between the results of our study and those of other studies originate from the differences in geographical areas, customs, cultures, diet or sample size. In addition, our study was carried out on kidney transplant recipients and not on other groups of immunocompromised patients.
One of the limitations of the present study was the small sample size. We also faced limitations of funding, which forced us to perform the tests on only one stool specimen of each participant.
Because the prevalence of intestinal fungal and parasitic infections is relatively high in kidney transplant recipients, it is recommended to evaluate these patients for these infections prior to administration of immunosuppressive drugs. It is also suggested to carry out similar studies with a larger sample size and different groups of immunocompromised patients to confirm the results of this study. Further investigations on the pathogenesis of these infections are needed as well.
| Acknowledgments | | |
The authors would like to acknowledge the kind co-operation extended by the staff of the Nephrology Ward and the Department of Parasitology and Mycology of Isfahan University of Medical Sciences, the staff of Noor Hospital Laboratory and Dr. Jalayer Parasitology Laboratory. Moreover, the kind assistance of Ms. Khojandi and Ms. Tousifian is much appreciated. This study was financially supported by the Isfahan University of Medical Sciences, Isfahan, Iran.
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Correspondence Address:
Afsoon Emami Naeini
Department of Nephrology, School of Medicine, Isfahan University of Medical Sciences, Isfahan
Iran
DOI: 10.4103/1319-2442.98110
[Table 1], [Table 2], [Table 3] |
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