Abstract
Purpose
Intestinal parasitic infections (IPIs) can result in high morbidity and mortality, particularly in immunocompromised patients. Infectious diseases are among the main causes of death in end-stage renal disease (ESRD) patients due to their impaired immune systems. The aim of this study was to determine the prevalence IPIs and their associated symptoms in ESRD patients.
Methods
In this case–control study, the fecal samples of 78 ESRD patients undergoing hemodialysis and 140 controls without any kidney problems were analyzed for intestinal parasites using direct-smear, formol-ether and modified Ziehl–Neelsen staining techniques.
Results
The difference in the prevalence of IPIs between ESRD patients (30.7 %) and the control group (10.7 %) was significant (OR = 3.7; 95 % CI = 1.8–7.61; P < 0.001). Blastocystis (14.1 %) and Cryptosporidium spp.(11.5 %) were the most common IPIs detected in ESRD patients, and the presence of Cryptosporidium spp. was significantly associated with diarrhea in ESRD patients (OR = 16; 95 % CI = 1.54–166.05; P < 0.05). Leukocytosis, diarrhea, weight loss, nausea/vomiting and bloating were also significantly higher in the hemodialysis group when compared with the control group.
Conclusion
The current study revealed a high prevalence of intestinal parasites and related clinical symptoms in ESRD patients undergoing hemodialysis. Since hemodialysis patients are immunocompromised and intestinal parasites can cause serious clinical complications, we suggest that stool examination for intestinal parasites, with an emphasis on detection of Cryptosporidium spp. and Blastocystis, should be incorporated into the routine clinical care for these patients. Measures for preventing the acquisition of IPIs are also recommended.
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References
Kato S, Chmielewski M, Honda H, Honda H, Pecoits-Filho R, Matsuo S, Yuzawa Y. Aspects of immune dysfunction in end-stage renal disease. Clin J Am Soc Nephrol. 2008;3:1526–33.
Drey N, Roderick P, Mullee M, Rogerson M. A population-based study of the incidence and outcomes of diagnosed chronic kidney disease. Am J Kidney Dis. 2003;42:677–84.
Tonelli M, Wiebe N, Culleton B, House A, Rabbat C, Fok M, McAlister F, Garg AX. Chronic kidney disease and mortality risk: a systematic review. J Am Soc Nephrol. 2006;17:2034–47.
Glorieux G, Vanholder R, Lameire N. Uraemic retention and apoptosis: what is the balance for the inflammatory status in uraemia? Eur J Clin Invest. 2003;33:631–4.
Haag-Weber M, Hörl WH. Dysfunction of polymorphonuclear leukocytes in uremia. Semin Nephrol. 1996;16:192–201.
World Health Organization. Division of control of tropical diseases (CTD), progress report 1996. Geneva: World Health Organization; 1997. p. 15–6.
Gumbo T, Sarbah S, Gangaidzo IT, Ortega Y, Sterling CR, Carville A, Tzipori S, Wiest PM. Intestinal parasites in patients with diarrhea and human immunodeficiency virus infection in Zimbabwe. Aids. 1999;13:819–21.
Sadraei J, Rizvi MA, Baveja UK. Diarrhea, CD4+ cell counts and opportunistic protozoa in Indian HIV-infected patients. Parasitol Res. 2005;97:270–3.
Sammet S, Wieser A, Müller S, Huber M, Schubert S, Seybold U. Triple worm infestation in an HIV-infected patient. Infection. 2013;41:1053–4.
Kulik RA, Falavigna DLM, Nishi L, Araujo SM. Blastocystis spp. and other intestinal parasites in hemodialysis patients. Braz J Infect Dis. 2008;12:338–41.
Gil FF, Barros MJ, Macedo NA, Júnior GEC, Redoan R, Busatti H, Gomes AM, Santos FGJ. Prevalence of intestinal parasitism and associated symptomatology among hemodialysis patients. Rev Inst Med Trop Sao Paulo. 2013;55:69–74.
Karadag G, Tamer GS, Dervisoglu E. Investigation of intestinal parasites in dialysis patients. Saudi Med J. 2013;34:714–8.
Bagheri P, Rakhshanpour A, Farhangnya M, Alizadeh H, Lotfi H, Sobhani H. A systematic review and meta-analysis of prevalence of intestinal parasitic infections in Iran (Article in Persian). Iranian J Infect Dis Trop Med. 2011;16:1–12.
Sardarian K, Hajilooi M, Maghsood A, Moghimbeigi A, Alikhani M. A study of the genetic variability of Blastocystishominis isolates in Hamadan, West of Iran. Jundishapur J Microbiol. 2012;5:555–9.
Sharifdini M, Kia EB, Ashrafi K, Hosseini M, Mirhendi H, Mohebali M, Kamranrashani B. An analysis of clinical characteristics of Strongyloidesstercoralis in 70 indigenous patients in Iran. Iran J Parasitol. 2014;9:155–62.
World Health Organization. Basic Laboratory methods in medical parasitology. Geneva: World Health Organization; 1991. p. 10–7.
Henricksen SA, Pohlenz JFL. Staining of Cryptosporidia by a modified Ziehl Neelsen technique. Acta Vet Scand. 1981;22:594–6.
Malaponte G, Libra M, Bevelacqua Y, Merito P, Fatuzzo P, Rapisarda F, Cristina M, Naselli G, Stivala F, Mazzarino MC, Castellino P. Inflammatory status in patients with chronic renal failure: the role of PTX3 and pro-inflammatory cytokines. Int J Mol Med. 2007;20:471–81.
Carrero JJ, Yilmaz MI, Lindholm B, Stenvinkel P. Cytokine dysregulation in chronic kidney disease: how can we treat it? Blood Purify. 2008;26:291–9.
de Jager DJ, Grootendorst DC, Jager KJ, van Dijk PC, Tomas LM, Ansell D, Collart F, Finne P, Heaf JG, De Meester J, Wetzels JF, Rosendaal FR, Dekker FW. Cardiovascular and noncardiovascular mortality among patients starting dialysis. JAMA J American Med Associat. 2009;302:1782–9.
Sarnak MJ, Jaber BL. Mortality caused by sepsis in patients with end-stage renal disease compared with the general population. Kidney Int. 2000;58:1758–64.
Olsson J. Leukocyte Function in High-Flux Hemodialysis. In: Carpi A, Donadio C, Tramonti G, editors. Progress in hemodialysis—from emergent biotechnology to clinical practice. InTech; 2011. p. 181–2. http://www.intechopen.com/books/progress-in-hemodialysis-from-emergent-biotechnology-to-clinical-practice/leukocyte-function-in-high-flux-hemodialysis. Accessed 15 June 2014.
Turkcapar N, Kutlay S, Nergizoglu G, Atli T, Duman N. Prevalence of Cryptosporidium infection in hemodialysis patients. Nephron. 2002;90:344–6.
Seyrafian S, Pestehchian N, Kerdegari M, Yousefi HA, Bastani B. Prevalence rate of Cryptosporidium infection in hemodialysis patients in Iran. Hemodial Int. 2006;10:375–9.
Ali MS, Mahmoud LA, Abaza BE, Ramadan MA. Intestinal spore-forming protozoa among patients suffering from renal failure. J Egypt Soc Parasitol. 2000;30:93–100.
Nkenfou CN, Nana CT, Payne VK. Intestinal parasitic infections in HIV Infected and non-infected patients in a low hiv prevalence region, West-Cameroon. PLoS One. 2013;8:e57914.
Seyrafian S, Pestechian N, Namdari N, Aviani M, Kerdegari M, Parvizian F, Kassaii L, Eshaghian A, Nasri H. Prevalence of parasitic infections in Iranian stable hemodialysis patients. Appl Med Inform. 2011;29:31–6.
Graczyk TK, Shiff CK, Tamang L, Munsaka F, Beitin AM, Moss WJ. The association of Blastocystishominis and Endolimax nana with diarrheal stools in Zambian school-age children. Parasitol Res. 2005;98:38–43.
Centers for Disease Control and Prevention (CDC). Blastocystishominis. Laboratory identification of parasites of public health concern. Last updated November 29, 2013. http://www.dpd.cdc.gov. Accessed 15 Jun 2014.
Anding K, Gross P, Rost JM, Allgaier D, Jacobs E. The influence of uraemia and haemodialysis on neutrophil phagocytosis and antimicrobial killing. Nephrol Dial Transplant. 2003;18:2067–73.
Praharaj I, Sujatha S, Ashwini MA, Parija SC. Co-infection with Nocardia asteroides complex and Strongyloides stercoralis in a patient with autoimmune hemolytic anemia. Infection. 2014;42:211–4.
Saraei M, Hosseinbigi B, Shahnazi M, Bijani B. Fatal Strongyloides hyper-infection in a patient with myasthenia gravis. Infection. 2014;42:1039–42.
Mokaddas EM, Shati S, Abdulla A, Nampoori NR, Iqbal J, Nair PM, et al. Fatal strongyloidiasis in three kidney recipients in Kuwait. Med Princ Pract. 2009;18:414–7.
Palau LA, Pankey GA. Strongyloides hyperinfection in a renal transplant recipient receiving cyclosporine: possible Strongyloides stercoralis transmission by kidney transplant. Am J Trop Med Hyg. 1997;57:413–5.
Hamilton KW, Abt PL, Rosenbach MA, Bleicher MB, Levine MS, Mehta J, et al. Donor-derived Strongyloides stercoralis infections in renal transplant recipients. Transplantation. 2011;91:1019–24.
Leapman SB, Rosenberg JB, Filo RS, Smith EJ. Strongyloides stercoralis in chronic renal failure: safe therapy with thiabendazole. South Med J. 1980;73:1400–2.
Keiser PB, Nutman TB. Strongyloides stercoralis in the immunocompromised population. Clin Microbiol Rev. 2004;17:208–17.
Buonfrate D, Requena-Mendez A, Angheben A, Muñoz J, Gobbi F, Van Den Ende J, et al. Severe strongyloidiasis: a systematic review of case reports. BMC Infect Dis. 2013;13:78.
Lau AH, Chang CW, Sabatini S. Hemodialysis clearance of metronidazole and its metabolites. Antimicrob Agents Chemother. 1986;29:235–8.
Acknowledgments
The authors are very thankful to Professor Graham Clark (Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine) for the time generously spent in thoroughly revising the manuscript. Also, we are very grateful to the 29-Bahman hospital laboratory staffs in Tabriz city, East Azerbaijan Province, Iran, for their technical assistance. Most importantly, the authors would like to thank all the hemodialysis patients and volunteered participants for giving permission to collect samples and participated in this study. We are thankful for the collaboration of protozoology unit of the Shahid Beheshti University of Medical Sciences.
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None of the above authors have any conflict of interest.
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Omrani, V.F., Fallahi, S., Rostami, A. et al. Prevalence of intestinal parasite infections and associated clinical symptoms among patients with end-stage renal disease undergoing hemodialysis. Infection 43, 537–544 (2015). https://doi.org/10.1007/s15010-015-0778-6
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DOI: https://doi.org/10.1007/s15010-015-0778-6