HIV/AIDS in Combination with Enterocytozoon bieneusi Infection
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Published
Apr 28, 2023
Abstract
Acquired immunodeficiency syndrome (AIDS) is a significant public health problem caused by infection with the human immunodeficiency virus (HIV). The most common cause of death in AIDS patients is opportunistic infection with various microorganisms. Intestinal protozoa, such as Enterocytozoon bieneusi, are prevalent yet difficult to treat. This review will provide an overview of HIV/AIDS mixed with Enterocytozoon bieneusi infection by discussing an introduction, epidemiology, detection methodology, and treatment strategies.
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Keywords
Human Immunodeficiency Virus, Acquired Immunodeficiency Syndrome, Opportunistic Infection, Enterocytozoon bieneusi, Outcomes
References
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3. Elfstrand L, Florén CH. Management of chronic diarrhea in HIV-infected patients: current treatment options, challenges and future directions. HIV AIDS (Auckl) 2010; 2:219-224. DOI: https://doi.org/10.2147/HIV.S13191
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6. Agholi M, Hatam GR, Motazedian MH. HIV/AIDS-associated opportunistic protozoal diarrhea. AIDS Res Hum Retroviruses 2013; 29(1):35-41. DOI: https://doi.org/10.1089/AID.2012.0119
7. Wang ZD, Liu Q, Liu HH, Li S, Zhang L, Zhao YK, Zhu XQ. Prevalence of Cryptosporidium, microsporidia and Isospora infection in HIV-infected people: A global systematic review and meta-analysis. Parasit Vectors 2018; 11(1):28. DOI: https://doi.org/10.1186/s13071-017-2558-x
8. Didier ES, Weiss LM. Microsporidiosis: Not just in AIDS patients. Curr Opin Infect Dis 2011; 24(5):490-495. DOI: https://doi.org/10.1097/QCO.0b013e32834aa152
9. Bass D, Czech L, Williams BAP, Berney C, Dunthorn M, Mahé F, Torruella G, Stentiford GD, Williams TA. Clarifying the relationships between microsporidia and cryptomycota. J Eukaryot Microbiol 2018; 65(6):773-782. DOI: https://doi.org/10.1111/jeu.12519
10. Han B, Weiss LM. Microsporidia: Obligate intracellular pathogens within the fungal kingdom. Microbiol Spectr 2017; 5(2). DOI: https://doi.org/10.1128/microbiolspec.FUNK-0018-2016
11. Robbertse B, Tatusova T. Fungal genome resources at NCBI. Mycology 2011; 2(3):142-160. DOI: https://doi.org/10.1080/21501203.2011.584576
12. Han B, Pan G, Weiss LM. Microsporidiosis in humans. Clin Microbiol Rev 2021; 34(4):e0001020. DOI: https://doi.org/10.1128/CMR.00010-20
13. Ramírez-Castillo FY, Loera-Muro A, Jacques M, Garneau P, Avelar-González FJ, Harel J, Guerrero-Barrera AL. Waterborne pathogens: Detection methods and challenges. Pathogens 2015; 4(2):307-334. DOI: https://doi.org/10.3390/pathogens4020307
14. Boshuizen JA, Reimerink JH, Korteland-van Male AM, van Ham VJ, Koopmans MP, Büller HA, Dekker J, Einerhand AW. Changes in small intestinal homeostasis, morphology, and gene expression during rotavirus infection of infant mice. J Virol 2003; 77(24):13005-13016. DOI: https://doi.org/10.1128/jvi.77.24.13005-13016.2003
15. Basta M, Annamaraju P. Bacterial Spores. [Updated 2023 Jan 30]. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2023. Available at: https://www.ncbi.nlm.nih.gov/books/NBK556071/
16. Stentiford GD, Becnel -J, Weiss LM, Keeling PJ, Didier ES, Williams BP, Bjornson S, Kent ML, Freeman MA, Brown MJF, Troemel ER, Roesel K, Sokolova Y, Snowden KF, Solter L. Microsporidia - Emergent pathogens in the global food chain. Trends Parasitol 2016; 32(4):336-348. DOI: https://doi.org/10.1016/j.pt.2015.12.004. Erratum in: Trends Parasitol 2016; 32(8):657.
17. Fadhilah A, Gabbar A, Bokhari AA. Microsporidium. [Updated 2022 Aug 29]. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2023. Available at: https://www.ncbi.nlm.nih.gov/books/NBK537166/
18. Graham JP, Leibler JH, Price LB, Otte JM, Pfeiffer DU, Tiensin T, Silbergeld EK. The animal-human interface and infectious disease in industrial food animal production: Rethinking biosecurity and biocontainment. Public Health Rep 2008; 123(3):282-299. DOI: https://doi.org/10.1177/003335490812300309
19. Fèvre EM, Bronsvoort BM, Hamilton KA, Cleaveland S. Animal movements and the spread of infectious diseases. Trends Microbiol 2006; 14(3):125-131. DOI: https://doi.org/10.1016/j.tim.2006.01.004
20. Merianos A. Surveillance and response to disease emergence. Curr Top Microbiol Immunol 2007; 315:477-509. DOI: https://doi.org/10.1007/978-3-540-70962-6_19
21. Liu CY, Hua-Jiang. Dead pigs scandal questions China’s public health policy. Lancet 2013; 381(9877):1539. DOI: https://doi.org/10.1016/S0140-6736(13)60768-0
22. Michlmayr D, Alves de Sousa L, Müller L, Jokelainen P, Ethelberg S, Vestergaard LS, Schjørring S, Mikkelsen S, Jensen CW, Rasmussen LD, Rune Stensvold C. Incubation period, spore shedding duration, and symptoms of Enterocytozoon bieneusi genotype c infection in a foodborne outbreak in Denmark, 2020. Clin Infect Dis 2022; 75(3):468-475. DOI: https://doi.org/10.1093/cid/ciab949
23. Bell R. ABC of sexual health: Homosexual men and women. BMJ 1999; 318(7181):452-455. DOI: https://doi.org/10.1136/bmj.318.7181.452
24. Nash AK, Auchtung TA, Wong MC, Smith DP, Gesell JR, Ross MC, Stewart CJ, Metcalf GA, Muzny DM, Gibbs RA, Ajami NJ, Petrosino JF. The gut mycobiome of the Human Microbiome Project healthy cohort. Microbiome 2017; 5(1):153. DOI: https://doi.org/10.1186/s40168-017-0373-4
25. Brenchley JM, Douek DC. HIV infection and the gastrointestinal immune system. Mucosal Immunol 2008; 1(1):23-30. DOI: https://doi.org/10.1038/mi.2007.1
26. Xu H, Wang X, Veazey RS. Mucosal immunology of HIV infection. Immunol Rev 2013; 254(1):10-33. DOI: https://doi.org/10.1111/imr.12072
27. Pokrovskiĭ VV, Iurin OG, Kravchenko AV, Potekaev NS, Gabrilovich DI, Makarova NIu, Potekaev SN. Pervyĭ sluchaĭ VICh-infektsii u grazhdanina SSSR [The first case of HIV infection in a citizen of the USSR]. Zh Mikrobiol Epidemiol Immunobiol 1992; 1992(11-12):19-22. Russian.
28. Wang ZD, Liu Q, Liu HH, Li S, Zhang L, Zhao YK, Zhu XQ. Prevalence of Cryptosporidium, microsporidia and Isospora infection in HIV-infected people: A global systematic review and meta-analysis. Parasit Vectors 2018; 11(1):28. DOI: https://doi.org/10.1186/s13071-017-2558-x
29. Embree J. The impact of HIV/AIDS on children in developing countries. Paediatr Child Health 2005; 10(5):261-263.
30. Pavlinac PB, Tickell KD, Walson JL. Management of diarrhea in HIV-affected infants and children. Expert Rev Anti Infect Ther 2015; 13(1):5-8. DOI: https://doi.org/10.1586/14787210.2015.981157
31. Carter PL, MacPherson DW, McKenzie RA. Modified technique to recover microsporidian spores in sodium acetate-acetic acid-formalin-fixed fecal samples by light microscopy and correlation with transmission electron microscopy. J Clin Microbiol 1996; 34(11):2670-2673. DOI: https://doi.org/10.1128/jcm.34.11.2670-2673.1996
32. Didier ES, Orenstein JM, Aldras A, Bertucci D, Rogers LB, Janney FA. Comparison of three staining methods for detecting microsporidia in fluids. J Clin Microbiol 1995; 33(12):3138-3145. DOI: https://doi.org/10.1128/jcm.33.12.3138-3145.1995
33. Kulkarni S, Patsute S, Chandane M, Risbud A. Performance of microscopy for detection of microsporidial spores from stool samples of HIV infected individuals with diarrhoea. Indian J Med Res 2011; 134(6):982-984. DOI: https://doi.org/10.4103/0971-5916.92646
34. Montoliu-Gaya L, Esquerda-Canals G, Bronsoms S, Villegas S. Production of an anti-Aβ antibody fragment in Pichia pastoris and in vitro and in vivo validation of its therapeutic effect. PLoS One 2017; 12(8):e0181480. DOI: https://doi.org/10.1371/journal.pone.0181480
35. Huang FC, Hsieh HY, Chang TC, Su SL, Tseng SL, Lai YH, Kuo MT. A DNA dot hybridization model for molecular diagnosis of parasitic keratitis. Mol Vis 2017; 23:614-623.
36. Clarridge JE 3rd. Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases. Clin Microbiol Rev 2004; 17(4):840-862. DOI: https://doi.org/10.1128/CMR.17.4.840-862.2004
37. Han B, Weiss LM. Therapeutic targets for the treatment of microsporidiosis in humans. Expert Opin Ther Targets 2018; 22(11):903-915. DOI: https://doi.org/10.1080/14728222.2018.1538360
38. Zhao Y, Wu Z, McGoogan JM, Shi CX, Li A, Dou Z, Ma Y, Qin Q, Brookmeyer R, Detels R, Montaner JSG. Immediate antiretroviral therapy decreases mortality among patients with high CD4 counts in China: A nationwide, retrospective cohort study. Clin Infect Dis 2018; 66(5):727-734. DOI: https://doi.org/10.1093/cid/cix878
39. Montaner JS, Lima VD, Harrigan PR, Lourenço L, Yip B, Nosyk B, Wood E, Kerr T, Shannon K, Moore D, Hogg RS, Barrios R, Gilbert M, Krajden M, Gustafson R, Daly P, Kendall P. Expansion of HAART coverage is associated with sustained decreases in HIV/AIDS morbidity, mortality and HIV transmission: The “HIV Treatment as Prevention” experience in a Canadian setting. PLoS One 2014; 9(2):e87872. DOI: https://doi.org/10.1371/journal.pone.0087872
40. Molina JM, Tourneur M, Sarfati C, Chevret S, de Gouvello A, Gobert JG, Balkan S, Derouin F; Agence Nationale de Recherches sur le SIDA 090 Study Group. Fumagillin treatment of intestinal microsporidiosis. N Engl J Med 2002; 346(25):1963-1969. DOI: https://doi.org/10.1056/NEJMoa012924
41. Dankner WM, Lindsey JC, Levin MJ; Pediatric AIDS Clinical Trials Group Protocol Teams 051, 128, 138, 144, 152, 179, 190, 220, 240, 245, 254, 300 and 327. Correlates of opportunistic infections in children infected with the human immunodeficiency virus managed before highly active antiretroviral therapy. Pediatr Infect Dis J 2001; 20(1):40-48. DOI: https://doi.org/10.1097/00006454-200101000-00008
42. Smith HV, Corcoran GD. New drugs and treatment for cryptosporidiosis. Curr Opin Infect Dis 2004; 17(6):557-564. DOI: https://doi.org/10.1097/00001432-200S412000-00008
2. Udeh EO, Obiezue RNN, Okafor FC, Ikele CB, Okoye IC, Otuu CA. Gastrointestinal parasitic infections and immunological status of HIV/AIDS coinfected individuals in Nigeria. Ann Glob Health 2019; 85(1):99. DOI: https://doi.org/10.5334/aogh.2554
3. Elfstrand L, Florén CH. Management of chronic diarrhea in HIV-infected patients: current treatment options, challenges and future directions. HIV AIDS (Auckl) 2010; 2:219-224. DOI: https://doi.org/10.2147/HIV.S13191
4. Justiz Vaillant AA, Naik R. HIV-1 Associated Opportunistic Infections. [Updated 2023 Jan 27]. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2023. Available at: https://www.ncbi.nlm.nih.gov/books/NBK539787/
5. Wilcox CM. Etiology and evaluation of diarrhea in AIDS: A global perspective at the millennium. World J Gastroenterol 2000; 6(2):177-186. DOI: https://doi.org/10.3748/wjg.v6.i2.177
6. Agholi M, Hatam GR, Motazedian MH. HIV/AIDS-associated opportunistic protozoal diarrhea. AIDS Res Hum Retroviruses 2013; 29(1):35-41. DOI: https://doi.org/10.1089/AID.2012.0119
7. Wang ZD, Liu Q, Liu HH, Li S, Zhang L, Zhao YK, Zhu XQ. Prevalence of Cryptosporidium, microsporidia and Isospora infection in HIV-infected people: A global systematic review and meta-analysis. Parasit Vectors 2018; 11(1):28. DOI: https://doi.org/10.1186/s13071-017-2558-x
8. Didier ES, Weiss LM. Microsporidiosis: Not just in AIDS patients. Curr Opin Infect Dis 2011; 24(5):490-495. DOI: https://doi.org/10.1097/QCO.0b013e32834aa152
9. Bass D, Czech L, Williams BAP, Berney C, Dunthorn M, Mahé F, Torruella G, Stentiford GD, Williams TA. Clarifying the relationships between microsporidia and cryptomycota. J Eukaryot Microbiol 2018; 65(6):773-782. DOI: https://doi.org/10.1111/jeu.12519
10. Han B, Weiss LM. Microsporidia: Obligate intracellular pathogens within the fungal kingdom. Microbiol Spectr 2017; 5(2). DOI: https://doi.org/10.1128/microbiolspec.FUNK-0018-2016
11. Robbertse B, Tatusova T. Fungal genome resources at NCBI. Mycology 2011; 2(3):142-160. DOI: https://doi.org/10.1080/21501203.2011.584576
12. Han B, Pan G, Weiss LM. Microsporidiosis in humans. Clin Microbiol Rev 2021; 34(4):e0001020. DOI: https://doi.org/10.1128/CMR.00010-20
13. Ramírez-Castillo FY, Loera-Muro A, Jacques M, Garneau P, Avelar-González FJ, Harel J, Guerrero-Barrera AL. Waterborne pathogens: Detection methods and challenges. Pathogens 2015; 4(2):307-334. DOI: https://doi.org/10.3390/pathogens4020307
14. Boshuizen JA, Reimerink JH, Korteland-van Male AM, van Ham VJ, Koopmans MP, Büller HA, Dekker J, Einerhand AW. Changes in small intestinal homeostasis, morphology, and gene expression during rotavirus infection of infant mice. J Virol 2003; 77(24):13005-13016. DOI: https://doi.org/10.1128/jvi.77.24.13005-13016.2003
15. Basta M, Annamaraju P. Bacterial Spores. [Updated 2023 Jan 30]. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2023. Available at: https://www.ncbi.nlm.nih.gov/books/NBK556071/
16. Stentiford GD, Becnel -J, Weiss LM, Keeling PJ, Didier ES, Williams BP, Bjornson S, Kent ML, Freeman MA, Brown MJF, Troemel ER, Roesel K, Sokolova Y, Snowden KF, Solter L. Microsporidia - Emergent pathogens in the global food chain. Trends Parasitol 2016; 32(4):336-348. DOI: https://doi.org/10.1016/j.pt.2015.12.004. Erratum in: Trends Parasitol 2016; 32(8):657.
17. Fadhilah A, Gabbar A, Bokhari AA. Microsporidium. [Updated 2022 Aug 29]. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2023. Available at: https://www.ncbi.nlm.nih.gov/books/NBK537166/
18. Graham JP, Leibler JH, Price LB, Otte JM, Pfeiffer DU, Tiensin T, Silbergeld EK. The animal-human interface and infectious disease in industrial food animal production: Rethinking biosecurity and biocontainment. Public Health Rep 2008; 123(3):282-299. DOI: https://doi.org/10.1177/003335490812300309
19. Fèvre EM, Bronsvoort BM, Hamilton KA, Cleaveland S. Animal movements and the spread of infectious diseases. Trends Microbiol 2006; 14(3):125-131. DOI: https://doi.org/10.1016/j.tim.2006.01.004
20. Merianos A. Surveillance and response to disease emergence. Curr Top Microbiol Immunol 2007; 315:477-509. DOI: https://doi.org/10.1007/978-3-540-70962-6_19
21. Liu CY, Hua-Jiang. Dead pigs scandal questions China’s public health policy. Lancet 2013; 381(9877):1539. DOI: https://doi.org/10.1016/S0140-6736(13)60768-0
22. Michlmayr D, Alves de Sousa L, Müller L, Jokelainen P, Ethelberg S, Vestergaard LS, Schjørring S, Mikkelsen S, Jensen CW, Rasmussen LD, Rune Stensvold C. Incubation period, spore shedding duration, and symptoms of Enterocytozoon bieneusi genotype c infection in a foodborne outbreak in Denmark, 2020. Clin Infect Dis 2022; 75(3):468-475. DOI: https://doi.org/10.1093/cid/ciab949
23. Bell R. ABC of sexual health: Homosexual men and women. BMJ 1999; 318(7181):452-455. DOI: https://doi.org/10.1136/bmj.318.7181.452
24. Nash AK, Auchtung TA, Wong MC, Smith DP, Gesell JR, Ross MC, Stewart CJ, Metcalf GA, Muzny DM, Gibbs RA, Ajami NJ, Petrosino JF. The gut mycobiome of the Human Microbiome Project healthy cohort. Microbiome 2017; 5(1):153. DOI: https://doi.org/10.1186/s40168-017-0373-4
25. Brenchley JM, Douek DC. HIV infection and the gastrointestinal immune system. Mucosal Immunol 2008; 1(1):23-30. DOI: https://doi.org/10.1038/mi.2007.1
26. Xu H, Wang X, Veazey RS. Mucosal immunology of HIV infection. Immunol Rev 2013; 254(1):10-33. DOI: https://doi.org/10.1111/imr.12072
27. Pokrovskiĭ VV, Iurin OG, Kravchenko AV, Potekaev NS, Gabrilovich DI, Makarova NIu, Potekaev SN. Pervyĭ sluchaĭ VICh-infektsii u grazhdanina SSSR [The first case of HIV infection in a citizen of the USSR]. Zh Mikrobiol Epidemiol Immunobiol 1992; 1992(11-12):19-22. Russian.
28. Wang ZD, Liu Q, Liu HH, Li S, Zhang L, Zhao YK, Zhu XQ. Prevalence of Cryptosporidium, microsporidia and Isospora infection in HIV-infected people: A global systematic review and meta-analysis. Parasit Vectors 2018; 11(1):28. DOI: https://doi.org/10.1186/s13071-017-2558-x
29. Embree J. The impact of HIV/AIDS on children in developing countries. Paediatr Child Health 2005; 10(5):261-263.
30. Pavlinac PB, Tickell KD, Walson JL. Management of diarrhea in HIV-affected infants and children. Expert Rev Anti Infect Ther 2015; 13(1):5-8. DOI: https://doi.org/10.1586/14787210.2015.981157
31. Carter PL, MacPherson DW, McKenzie RA. Modified technique to recover microsporidian spores in sodium acetate-acetic acid-formalin-fixed fecal samples by light microscopy and correlation with transmission electron microscopy. J Clin Microbiol 1996; 34(11):2670-2673. DOI: https://doi.org/10.1128/jcm.34.11.2670-2673.1996
32. Didier ES, Orenstein JM, Aldras A, Bertucci D, Rogers LB, Janney FA. Comparison of three staining methods for detecting microsporidia in fluids. J Clin Microbiol 1995; 33(12):3138-3145. DOI: https://doi.org/10.1128/jcm.33.12.3138-3145.1995
33. Kulkarni S, Patsute S, Chandane M, Risbud A. Performance of microscopy for detection of microsporidial spores from stool samples of HIV infected individuals with diarrhoea. Indian J Med Res 2011; 134(6):982-984. DOI: https://doi.org/10.4103/0971-5916.92646
34. Montoliu-Gaya L, Esquerda-Canals G, Bronsoms S, Villegas S. Production of an anti-Aβ antibody fragment in Pichia pastoris and in vitro and in vivo validation of its therapeutic effect. PLoS One 2017; 12(8):e0181480. DOI: https://doi.org/10.1371/journal.pone.0181480
35. Huang FC, Hsieh HY, Chang TC, Su SL, Tseng SL, Lai YH, Kuo MT. A DNA dot hybridization model for molecular diagnosis of parasitic keratitis. Mol Vis 2017; 23:614-623.
36. Clarridge JE 3rd. Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases. Clin Microbiol Rev 2004; 17(4):840-862. DOI: https://doi.org/10.1128/CMR.17.4.840-862.2004
37. Han B, Weiss LM. Therapeutic targets for the treatment of microsporidiosis in humans. Expert Opin Ther Targets 2018; 22(11):903-915. DOI: https://doi.org/10.1080/14728222.2018.1538360
38. Zhao Y, Wu Z, McGoogan JM, Shi CX, Li A, Dou Z, Ma Y, Qin Q, Brookmeyer R, Detels R, Montaner JSG. Immediate antiretroviral therapy decreases mortality among patients with high CD4 counts in China: A nationwide, retrospective cohort study. Clin Infect Dis 2018; 66(5):727-734. DOI: https://doi.org/10.1093/cid/cix878
39. Montaner JS, Lima VD, Harrigan PR, Lourenço L, Yip B, Nosyk B, Wood E, Kerr T, Shannon K, Moore D, Hogg RS, Barrios R, Gilbert M, Krajden M, Gustafson R, Daly P, Kendall P. Expansion of HAART coverage is associated with sustained decreases in HIV/AIDS morbidity, mortality and HIV transmission: The “HIV Treatment as Prevention” experience in a Canadian setting. PLoS One 2014; 9(2):e87872. DOI: https://doi.org/10.1371/journal.pone.0087872
40. Molina JM, Tourneur M, Sarfati C, Chevret S, de Gouvello A, Gobert JG, Balkan S, Derouin F; Agence Nationale de Recherches sur le SIDA 090 Study Group. Fumagillin treatment of intestinal microsporidiosis. N Engl J Med 2002; 346(25):1963-1969. DOI: https://doi.org/10.1056/NEJMoa012924
41. Dankner WM, Lindsey JC, Levin MJ; Pediatric AIDS Clinical Trials Group Protocol Teams 051, 128, 138, 144, 152, 179, 190, 220, 240, 245, 254, 300 and 327. Correlates of opportunistic infections in children infected with the human immunodeficiency virus managed before highly active antiretroviral therapy. Pediatr Infect Dis J 2001; 20(1):40-48. DOI: https://doi.org/10.1097/00006454-200101000-00008
42. Smith HV, Corcoran GD. New drugs and treatment for cryptosporidiosis. Curr Opin Infect Dis 2004; 17(6):557-564. DOI: https://doi.org/10.1097/00001432-200S412000-00008
How to Cite
Ahmed, A. (2023). HIV/AIDS in Combination with Enterocytozoon bieneusi Infection. Science Insights, 42(4), 891–895. https://doi.org/10.15354/si.23.re285
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