Advertisement

Parasitology Research

, Volume 118, Issue 10, pp 3061–3066 | Cite as

Isolation, identification, and phylogenetic analysis of potentially pathogenic free-living amoebae isolated from nasal and oral mucosa of HIV/AIDS patients in Iran

  • Zahra Arab-Mazar
  • Maryam NiyyatiEmail author
  • Zohreh Lasjerdi
  • Adel Spotin
  • Ilad Alavi Darzam
  • Latif Gachkar
Protozoology - Original Paper

Abstract

The burden of HIV/AIDS in Iran is not as high as in the other countries with high prevalence; however, the number of cases of HIV/AIDs is increasing in this region. According to a recent report, Iran had 5000 (1400–13,000) new cases of HIV infection with 4000 (2500–6200) AIDS-related deaths. Individuals affected by HIV/AIDS are highly susceptible for developing opportunistic infections, e.g. the cerebral complications related to pathogenic free-living amoebae and colonization of free-living amoebae (FLA) can be a serious hazard for patients living with HIV/AIDS. In the present study, a total of 70 oral and nasal mucosal samples were obtained from HIV/AIDS patients referred to the reference hospitals in Iran and tested for the presence of potentially pathogenic FLA using culture and PCR/sequencing-based methods. To discern the taxonomic status of Acanthamoeba genotypes a maximum likelihood phylogenetic tree was constructed and tolerance assays were performed for the positive Acanthamoeba strains. Among the patients with HIV/AIDS referred to the reference hospitals from 2017 to 2019, 7.1% were found positive for pathogenic free-living amoebae. Three strains (HA3, HA4, and HA5) belonged to the T4 genotype, one strain (HA1) was related to the T5 genotype assigned as A. lenticulata, and another strain (HA2) had high homology to Vermamoeba vermiformis. The tolerance assay used for Acanthamoeba strains (HA1, HA3, and HA4) classified these amoebae as highly pathogenic strains. For the most part, the encephalitis cases occurring in HIV/AIDS patients in Iran remain undiagnosed due to lack of awareness of the practitioners on the available diagnostic tools for this lethal infection; therefore, the true incidence of GAE in this region is unknown. A possible colonization with FLA should be considered in the differential diagnosis of suspected cases of CNS infections among HIV/AIDS patients. This study is the first worldwide comprehensive study attempting to isolate and identify the FLA colonization in HIV/AIDS patients. This study highlights the fact that clinicians should be aware of the differential diagnosis of cerebral disease related to FLA in patients with HIV/AIDS.

Keywords

HIV/AIDS patients Free-living amoebae Iran 

Notes

Acknowledgements

Thanks are due to Shahid Beheshti University educational hospitals for their kind assistance.

Funding information

This study was funded by the Infectious Diseases and Tropical Medicine Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran (grant number: 12278).

Compliance with ethical standards

The Ethics Committee of Shahid Beheshti University of Medical Sciences in Iran approved this study (ethics committee code: 1396.1122).

References

  1. Arnalich-Montiel F, Reyes-Batlle M, López-Vélez R, Lorenzo-Morales J (2018) Treatment of intraocular spread of acanthamoeba after tectonic corneal graft in acanthamoeba keratitis. Eye 32(7):1286–1287CrossRefGoogle Scholar
  2. Bowen LN, Smith B, Reich D, Quezado M, Nath A (2016) HIV-associated opportunistic CNS infections: pathophysiology, diagnosis and treatment. Nat Rev Neurol 12(11):662–674CrossRefGoogle Scholar
  3. Cabello-Vílchez AM, Núñez-Ato RG (2018) Isolation and molecular characterization of nontuberculous mycobacteria in the water distribution system in a hospital of Lima (perú). Biosalud 17(2):7–24Google Scholar
  4. Cabello-Vílchez AM, Martín-Navarro CM, López-Arencibia A, Reyes-Batlle M, González AC, Guerra H, Gotuzzo E, Valladares B, Piñero JE, Lorenzo-Morales J (2014) Genotyping of potentially pathogenic Acanthamoeba strains isolated from nasal swabs of healthy individuals in Peru. Acta Trop 130:7–10CrossRefGoogle Scholar
  5. Carter WW, Gompf SG, Toney JF (2004) Patient with AIDS; a possible role for early antiretroviral therapy. AIDS ReadGoogle Scholar
  6. Centeno M, Rivera F, Cerva L, Tsutsumi V, Gallegos E, Calderón A, Ortiz R, Bonilla P, Ramírez E, Suárez G (1996) Hartmannella vermiformis isolated from the cerebrospinal fluid of a young male patient with meningoencephalitis and bronchopneumonia. Arch Med Res 27(4):579–586Google Scholar
  7. El Sahly H, Udayamurthy M, Parkerson G, Hasbun R (2017) Survival of an AIDS patient after infection with Acanthamoeba sp. of the central nervous system. Infection 45(5):715–718CrossRefGoogle Scholar
  8. Geith S, Walochnik J, Prantl F, Sack S, Eyer F (2018) Lethal outcome of granulomatous acanthamoebic encephalitis in a man who was human immunodeficiency virus-positive: a case report. J Med Case Rep 12(1):201CrossRefGoogle Scholar
  9. Hajialilo E, Niyyati M, Solaymani M, Rezaeian M (2015) Pathogenic free-living amoebae isolated from contact lenses of keratitis patients. Iran J Parasitol 10(4):541Google Scholar
  10. Hajialilo E, Behnia M, Tarighi F, Niyyati M, Rezaeian M (2016) Isolation and genotyping of Acanthamoeba strains (T4, T9, and T11) from amoebic keratitis patients in Iran. Parasitol Res 115(8):3147–3151CrossRefGoogle Scholar
  11. Joulaei H, Lankarani KB, Kazerooni PA, Marzban M (2017) Number of HIV-infected cases in Iran: true or just an iceberg. Indian J Sex Transm Dis AIDS 38(2):157CrossRefGoogle Scholar
  12. Khan NA (2001) Pathogenicity, morphology, and differentiation of Acanthamoeba. Curr Microbiol 43(6):391–395CrossRefGoogle Scholar
  13. Khan NA (2006) Acanthamoeba: biology and increasing importance in human health. FEMS Microbiol Rev 30(4):564–595CrossRefGoogle Scholar
  14. Khan NA, Siddiqui R (2009) Acanthamoeba affects the integrity of human brain microvascular endothelial cells and degrades the tight junction proteins. Int J Parasitol 39(14):1611–1616CrossRefGoogle Scholar
  15. Kinnear F (2003) Cytopathogenicity of Acanthamoeba, Vahlkampfia and Hartmannella: quantative & qualitative in vitro studies on keratocytes. J Inf Secur 46(4):228–237Google Scholar
  16. Kong H-H, Chung D-I (1996) PCR and RFLP variation of conserved region of small subunit ribosomal DNA among Acanthamoeba isolates assigned to either A. castellanii or A. polyphaga. Korean J Parasitol 34:127-134Google Scholar
  17. Lasjerdi Z, Niyyati M, Haghighi A, Shahabi S, Biderouni FT, Taghipour N, Eftekhar M, Nazemalhosseini Mojarad E (2011) Potentially pathogenic free-living amoebae isolated from hospital wards with immunodeficient patients in Tehran, Iran. Parasitol Res 109(3):575–580CrossRefGoogle Scholar
  18. Lass A, Szostakowska B, Idzińska A, Chomicz L (2014) The first genotype determination of Acanthamoeba potential threat to human health, isolated from natural water reservoirs in Poland. Parasitol Res 113(7):2693–2699CrossRefGoogle Scholar
  19. Lass A, Guerrero M, Li X, Karanis G, Ma L, Karanis P (2017) Detection of Acanthamoeba spp. in water samples collected from natural water reservoirs, sewages, and pharmaceutical factory drains using LAMP and PCR in China. Sci Total Environ 584:489–494CrossRefGoogle Scholar
  20. Lorenzo-Morales J, Martín-Navarro CM, López-Arencibia A, Arnalich-Montiel F, Piñero JE, Valladares B (2013) Acanthamoeba keratitis: an emerging disease gathering importance worldwide? Trends Parasitol 29(4):181–187CrossRefGoogle Scholar
  21. MacLean RC, Hafez N, Tripathi S, Childress CG, Ghatak NR, Marciano-Cabral F (2007) Identification of Acanthamoeba sp. in paraffin-embedded CNS tissue from an HIV+ individual by PCR. Diagn Microbiol Infect Dis 57(3):289–294CrossRefGoogle Scholar
  22. Marciano-Cabral F, Cabral G (2003) Acanthamoeba spp. as agents of disease in humans. Clin Microbiol Rev 16(2):273–307CrossRefGoogle Scholar
  23. Marciano-Cabral F, MacLean R, Mensah A, LaPat-Polasko L (2003) Identification of Naegleria fowleri in domestic water sources by nested PCR. Appl Environ Microbiol 69(10):5864–5869CrossRefGoogle Scholar
  24. Martinez MS et al (2000) Granulomatous amebic encephalitis in a patient with AIDS: isolation of Acanthamoeba sp. group II from brain tissue and successful treatment with sulfadiazine and fluconazole. J Clin Microbiol 38(10):3892–3895Google Scholar
  25. Memari F, Niyyati M, Haghighi A, Tabaei SJS, Lasjerdi Z (2015) Occurrence of pathogenic Acanthamoeba genotypes in nasal swabs of cancer patients in Iran. Parasitol Res 114(5):1907–1912CrossRefGoogle Scholar
  26. Memari F, Niyyati M, Joneidi Z (2017) Pathogenic Acanthamoeba T4 genotype isolated from mucosal tissue of a patient with HIV infection: a case report. Iran J Parasitol 12(1):143Google Scholar
  27. Movahedi Z, Shokrollahi MR, Aghaali M, Heydari H (2012) Primary amoebic meningoencephalitis in an Iranian infant. Case Rep Med 2012:1–4CrossRefGoogle Scholar
  28. Niyyati M, Rezaeian M (2015) Current status of Acanthamoeba in Iran: a narrative review article. Iran J Parasitol 10(2):157–163Google Scholar
  29. Niyyati M, Lorenzo-Morales J, Rezaie S, Rahimi F, Mohebali M, Maghsood AH, Motevalli-Haghi A, Martín-Navarro CM, Farnia S, Valladares B, Rezaeian M (2009) Genotyping of Acanthamoeba isolates from clinical and environmental specimens in Iran. Exp Parasitol 121(3):242–245CrossRefGoogle Scholar
  30. Niyyati M, Saberi R, Lorenzo-Morales J, Salehi R (2016) High occurrence of potentially-pathogenic free-living amoebae in tap water and recreational water sources in South-West Iran. Trop Biomed 33(1):95–101Google Scholar
  31. Niyyati M, Arab-Mazar Z, Lasjerdi Z, Lorenzo-Morales J, Espotin A, Yadegarynia D, Gachkar L, Rahmati Roodsari S (2017) Molecular characterization of Acanthamoeba strains isolated from the oral cavity of hemodialysis patients in Iran. Parasitol Res 116(11):2965–2969CrossRefGoogle Scholar
  32. Ong TYY, Khan NA, Siddiqui R (2017) Brain-eating amoebae: predilection sites in the brain and disease outcome. J Clin Microbiol 55(7):1989–1997CrossRefGoogle Scholar
  33. Ovrutsky AR, Chan ED, Kartalija M, Bai X, Jackson M, Gibbs S, Falkinham JO III, Iseman MD, Reynolds PR, McDonnell G, Thomas V (2013) Cooccurrence of free-living amoebae and nontuberculous Mycobacteria in hospital water networks, and preferential growth of Mycobacterium avium in Acanthamoeba lenticulata. Appl Environ Microbiol 79(10):3185–3192CrossRefGoogle Scholar
  34. Pietrucha-Dilanchian P, Chan JC, Castellano-Sanchez A, Hirzel A, Laowansiri P, Tuda C, Visvesvara GS, Qvarnstrom Y, Ratzan KR (2012) Balamuthia mandrillaris and Acanthamoeba amebic encephalitis with neurotoxoplasmosis coinfection in a patient with advanced HIV infection. J Clin Microbiol 50(3):1128–1131CrossRefGoogle Scholar
  35. Sente C, et al. (2016) Xenic cultivation and genotyping of pathogenic free-living amoeba from public water supply sources in Uganda. New Journal of Science 2016Google Scholar
  36. Sisson DD (1995) Acute and short-term hemodynamic, echocardiography, and clinical effects of enalapril maleate in dogs with naturally acquired heart failure: results of the Invasive Multicenter PROspective Veterinary Evaluation of Enalapril Study: the IMPROVE study group. J Vet Intern Med 9(4):234–242CrossRefGoogle Scholar
  37. Todd CD et al (2015) Isolation and molecular characterization of Acanthamoeba genotypes in recreational and domestic water sources from Jamaica, West Indies. J Water Health 13(3):909–919CrossRefGoogle Scholar
  38. Visvesvara GS, Moura H, Schuster FL (2007) Pathogenic and opportunistic free-living amoebae: Acanthamoeba spp., Balamuthia mandrillaris, Naegleria fowleri, and Sappinia diploidea. FEMS Immunol Med Microbiol 50(1):1–26CrossRefGoogle Scholar
  39. Yohannan B, Feldman M (2019) Fatal Balamuthia mandrillaris Encephalitis. Case Rep Infect Dis 2019:1–5Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Medical Parasitology and Mycology, School of Public HealthTehran University of Medical SciencesTehranIran
  2. 2.Infectious Diseases and Tropical Medicine Research CenterShahid Beheshti University of Medical SciencesTehranIran
  3. 3.Department of Medical Parasitology and Mycology, School of MedicineShahid Beheshti University of Medical SciencesTehranIran
  4. 4.Immunology Research CenterTabriz University of Medical SciencesTabrizIran
  5. 5.Clinical Research Development Center, Loghman Hakim HospitalShahid Beheshti University of Medical SciencesTehranIran

Personalised recommendations