Microscopic and Molecular Investigation of Intestinal Microsporidia in HIV + /AIDS and Cancer Patients Undergoing Chemotherapy in Mazandaran Province, North of Iran.
Cancer
E. bieneusi
Encephalitozoon spp.
Genotyping
HIV + /AIDS
Journal
Acta parasitologica
ISSN: 1896-1851
Titre abrégé: Acta Parasitol
Pays: Switzerland
ID NLM: 9301947
Informations de publication
Date de publication:
Sep 2023
Sep 2023
Historique:
received:
15
04
2023
accepted:
20
07
2023
medline:
29
8
2023
pubmed:
11
8
2023
entrez:
11
8
2023
Statut:
ppublish
Résumé
The aim of this study was to identify Enterocytozoon bieneusi and Encephalitozoon spp. in fecal samples of HIV + /AIDS and cancer patients undergoing chemotherapy, and comparing the results to healthy individuals in Mazandaran province, north of Iran. Stool samples were collected from 50 HIV + /AIDS patients, 50 cancer patients, and 50 healthy samples referred to medical centers in north of Iran. Stool samples were kept in 2.5% potassium dichromate at 4 °C, and stained by modified trichrome for light microscopy examination. The multiplex/nested-PCR targeted the small subunit ribosomal RNA (SSU rRNA) gene. To characterize genotypes, the nested PCR products sequenced by Bioneer Company and was subjected to phylogenetic analyses. Ten of 50 samples (20%) of HIV + /AIDS patients, 5 of 50 samples (10%) of cancer patients, and 1 of healthy individuals (2%) were microscopically positive. From 50 HIV + / AIDS patients, E. bieneusi and Encephalitozoon spp. were detected in 10 (20%) and 6 (12%) cases, respectively. Furthermore, among cancer patients, 7 (14%) and 2 (4%) cases were E. bieneusi and Encephalitozoon spp., respectively. Out of 50 samples of healthy individuals, only 3 (6%) cases of E. bieneusi were observed. The genotypes D and M were detected among positive samples of E. bieneusi. E. bieneusi and then Encephalitozoon spp. are common intestinal microsporidia in HIV + /AIDS patients and cancer patients undergoing chemotherapy in Mazandaran province. E. bieneusi genotype D seems to be the predominant genotype in Mazandaran province. Due to the considerable prevalence of intestinal microsporidia, physicians are advised to pay more attention to this opportunistic infection in high-risk groups.
Sections du résumé
BACKGROUND
BACKGROUND
The aim of this study was to identify Enterocytozoon bieneusi and Encephalitozoon spp. in fecal samples of HIV + /AIDS and cancer patients undergoing chemotherapy, and comparing the results to healthy individuals in Mazandaran province, north of Iran.
METHODS
METHODS
Stool samples were collected from 50 HIV + /AIDS patients, 50 cancer patients, and 50 healthy samples referred to medical centers in north of Iran. Stool samples were kept in 2.5% potassium dichromate at 4 °C, and stained by modified trichrome for light microscopy examination. The multiplex/nested-PCR targeted the small subunit ribosomal RNA (SSU rRNA) gene. To characterize genotypes, the nested PCR products sequenced by Bioneer Company and was subjected to phylogenetic analyses.
RESULTS
RESULTS
Ten of 50 samples (20%) of HIV + /AIDS patients, 5 of 50 samples (10%) of cancer patients, and 1 of healthy individuals (2%) were microscopically positive. From 50 HIV + / AIDS patients, E. bieneusi and Encephalitozoon spp. were detected in 10 (20%) and 6 (12%) cases, respectively. Furthermore, among cancer patients, 7 (14%) and 2 (4%) cases were E. bieneusi and Encephalitozoon spp., respectively. Out of 50 samples of healthy individuals, only 3 (6%) cases of E. bieneusi were observed. The genotypes D and M were detected among positive samples of E. bieneusi.
CONCLUSIONS
CONCLUSIONS
E. bieneusi and then Encephalitozoon spp. are common intestinal microsporidia in HIV + /AIDS patients and cancer patients undergoing chemotherapy in Mazandaran province. E. bieneusi genotype D seems to be the predominant genotype in Mazandaran province. Due to the considerable prevalence of intestinal microsporidia, physicians are advised to pay more attention to this opportunistic infection in high-risk groups.
Identifiants
pubmed: 37566357
doi: 10.1007/s11686-023-00704-y
pii: 10.1007/s11686-023-00704-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
690-698Informations de copyright
© 2023. The Author(s) under exclusive licence to Witold Stefański Institute of Parasitology, Polish Academy of Sciences.
Références
Ghoyounchi R, Mahami-Oskouei M, Rezamand A, Spotin A, Aminisani N, Nami S, Pirestani M, Berahmat R, Madadi S (2019) Molecular phylodiagnosis of Enterocytozoon bieneusi and Encephalitozoon intestinalis in children with cancer: microsporidia in malignancies as an emerging opportunistic infection. Acta Parasitol 64(1):103–111. https://doi.org/10.2478/s11686-01800012-w
doi: 10.2478/s11686-01800012-w
pubmed: 30644064
Ghoyounchi R, Ahmadpour E, Spotin A, Mahami-Oskouei M, Rezamand A, Aminisani N, Ghojazadeh M, Berahmat R, Mikaeili-Galeh T (2017) Microsporidiosis in Iran: a systematic review and meta-analysis. Asian Pac J Trop Med 10(4):341–350. https://doi.org/10.1016/j.apjtm.2017.03.017
doi: 10.1016/j.apjtm.2017.03.017
pubmed: 28552104
Tavalla M, Kazemi F, Mardani-Kateki M, Abdizadeh R (2018) Molecular diagnosis of Enterocytozoon bieneusi and Encephalitozoon spp. in wild rats of southwest of Iran. Jundishapur J Microbiol. https://doi.org/10.1016/j.jiph.2017.07.028
doi: 10.1016/j.jiph.2017.07.028
Weber R, Bryan RT, Schwartz DA, Owen RL (1994) Human microsporidial infections. J Clin Microbiol 7(4):426–461. https://doi.org/10.1128/CMR.7.4.426
doi: 10.1128/CMR.7.4.426
Mirjalali H, Mohebali M, Mirhendi H, Gholami R, Keshavarz H, Meamar AR, Rezaeian M (2014) Emerging intestinal microsporidia infection in HIV+/AIDS patients in Iran: microscopic and molecular detection. Iran J Parasitol 9(2):149
pubmed: 25848379
pmcid: 4386033
Pirestani M, Sadraei J, Forouzandeh M (2013) Molecular characterization and genotyping of human related microsporidia in free-ranging and captive pigeons of Tehran Iran. Infect Genet Evol 20:495–499. https://doi.org/10.1016/j.meegid.2013.10.007
doi: 10.1016/j.meegid.2013.10.007
pubmed: 24427811
Karimi K, Mirjalali H, Niyyati M, Haghighi A, Pourhoseingholi MA, Sharifdini M, Naderi N, Zali MR (2020) Molecular epidemiology of Enterocytozoon bieneusi and Encephalitozoon sp., among immunocompromised and immunocompetent subjects in Iran. Microb Pathog 141:103988. https://doi.org/10.1016/j.micpath.2020.103988
doi: 10.1016/j.micpath.2020.103988
pubmed: 31972268
Mirjalali H, Mirhendi H, Meamar AR, Mohebali M, Askari Z, Mirsamadi ES, Rezaeian M (2015) Genotyping and molecular analysis of Enterocytozoon bieneusi isolated from immunocompromised patients in Iran. Infect Genet Evol 36:244–249. https://doi.org/10.1016/j.meegid.2015.09.022
doi: 10.1016/j.meegid.2015.09.022
pubmed: 26423670
Scaglia M, Gatti S, Bruno A, Bernuzzi A, Cevini C, Maserati R (2001) Pathogenic protozoans in man differential characterization of Entamoeba histolytica/Entamoeba dispar complex, Acanthamoeba spp. Microsporidia. Parassitologia 43:37–43
pubmed: 12078476
Karim MR, Dong H, Li T, Yu F, Li D, Zhang L, Li J, Wang R, Li S, Li X (2015) Predomination and new genotypes of Enterocytozoon bieneusi in captive nonhuman primates in zoos in China: high genetic diversity and zoonotic significance. PLoS ONE 10(2):e0117991. https://doi.org/10.1371/journal.pone.0117991
doi: 10.1371/journal.pone.0117991
pubmed: 25705879
pmcid: 4338232
Li W, Xiao L (2019) Multilocus sequence typing and population genetic analysis of Enterocytozoon bieneusi host specificity and its impacts on public health. Front Genet 10:307. https://doi.org/10.3389/fgene.2019.00307
doi: 10.3389/fgene.2019.00307
pubmed: 31001333
pmcid: 6454070
Punpoowong B, Pitisuttithum P, Chindanond D, Phiboonnakit D, Leelasuphasri S (1995) Microsporidium: modified technique for light microscopic diagnosis. J Med Assoc Thai 78(5):251–254. https://doi.org/10.1128/JCM.40.6.1892-1901.2002
doi: 10.1128/JCM.40.6.1892-1901.2002
pubmed: 7561548
Garcia LS (2002) Laboratory identification of the microsporidia. J Clin Microbiol 40(6):1892–1901. https://doi.org/10.1128/JCM.40.6.1892-1901
doi: 10.1128/JCM.40.6.1892-1901
pubmed: 12037040
pmcid: 130667
Sulaiman IM, Fayer R, Lal AA, Trout JM, Schaefer FW III, Xiao L (2003) Molecular characterization of microsporidia indicates that wild mammals harbor host-adapted Enterocytozoon spp. as well as human-pathogenic Enterocytozoon bieneusi. Appl Environ Microbiol 69(8):4495–4501. https://doi.org/10.1128/AEM.69.8.4495-4501.2003
doi: 10.1128/AEM.69.8.4495-4501.2003
pubmed: 12902234
pmcid: 169096
Tavalla M, Mardani-Kateki M, Abdizadeh R, Nashibi R, Rafie A, Khademvatan S (2017) Molecular identification of Enterocytozoon bieneusi and Encephalitozoon spp. in immunodeficient patients in Ahvaz. Southwest Iran Acta Trop 172:107–112. https://doi.org/10.1016/j.actatropica.2017.04.015
doi: 10.1016/j.actatropica.2017.04.015
pubmed: 28438442
Ryan NJ, Sutherland G, Coughlan K, Globan M, Doultree J, Marshall J, Baird R, Pedersen J, Dwyer B (1993) A new trichrome-blue stain for detection of microsporidial species in urine, stool, and nasopharyngeal specimens. J Clin Microbiol 31(12):3264–3269. https://doi.org/10.1128/jcm.31.12.3264-3269.1993
doi: 10.1128/jcm.31.12.3264-3269.1993
pubmed: 7508457
pmcid: 266395
Katzwinkel-Wladarsch S, Lieb M, Heise W, Löscher T, Rinder H (1996) Direct amplification and species determination of microsporidian DNA from stool specimens. Trop Med Int Health 1(3):373–378. https://doi.org/10.1046/j.1365-3156.1996.d01-51.x
doi: 10.1046/j.1365-3156.1996.d01-51.x
pubmed: 8673842
Panarelli NC, Yantiss RK (2018) Inflammatory and infectious manifestations of immunodeficiency in the gastrointestinal tract. Mod Pathol 31(6):844–861. https://doi.org/10.1038/s41379-018-0015-9
doi: 10.1038/s41379-018-0015-9
pubmed: 29403083
Han B, Pan G, Weiss LM (2021) Microsporidiosis in humans. Clin Microbiol Rev 34(4):e00010-00020. https://doi.org/10.1128/CMR.00010-20
doi: 10.1128/CMR.00010-20
pubmed: 34190570
pmcid: 8404701
Taghipour A, Bahadory S, Khazaei S (2020) A systematic review and meta-analysis on the global prevalence of microsporidia infection among dogs: a zoonotic concern. Trop Med Health 48(1):1–10. https://doi.org/10.1186/s41182-020-00265-0
doi: 10.1186/s41182-020-00265-0
Qiu L, Xia W, Li W, Ping J, Ding S, Liu H (2019) The prevalence of microsporidia in China: a systematic review and meta-analysis. Sci Rep 9(1):1–9. https://doi.org/10.1038/s41598-019-39290-3
doi: 10.1038/s41598-019-39290-3
Wang Z-D, Liu Q, Liu H-H, Li S, Zhang L, Zhao Y-K, Zhu X-Q (2018) Prevalence of Cryptosporidium, microsporidia and Isospora infection in HIV-infected people: a global systematic review and meta-analysis. Parasit Vectors 11(1):1–19. https://doi.org/10.1186/s13071-017-2558-x
doi: 10.1186/s13071-017-2558-x
pubmed: 29291748
pmcid: 5748956
Çetinkaya Ü, Caner A (2020) Prevalence of Microsporidiosis in different hosts in Turkey: a meta-analysis. Turkiye Parazitol Derg 44(4):232. https://doi.org/10.4274/tpd.galenos.2020.7093
doi: 10.4274/tpd.galenos.2020.7093
pubmed: 33269566
Li W, Feng Y, Xiao L (2020) Diagnosis and molecular typing of Enterocytozoon bieneusi: the significant role of domestic animals in transmission of human microsporidiosis. Res Vet Sci 133:251–261. https://doi.org/10.1016/j.rvsc.2020.09.030
doi: 10.1016/j.rvsc.2020.09.030
pubmed: 33035931
Behravan M, Yusuf MA, Solgi R, Haghighi A (2021) Prevalence of intestinal microsporidiosis by morphological and molecular methods in eastern Iran. Gene Rep 24:101296. https://doi.org/10.1016/j.genrep.2021.101296
doi: 10.1016/j.genrep.2021.101296
Desoubeaux G, Nourrisson C, Moniot M, De Kyvon M-A, Bonnin V, De La Bretonniére ME, Morange V, Bailly É, Lemaignen A, Morio F (2019) Genotyping approach for potential common source of Enterocytozoon bieneusi infection in hematology unit. Emerg Infect Dis 25(9):1625. https://doi.org/10.3201/eid2509.190311
doi: 10.3201/eid2509.190311
pubmed: 31441425
pmcid: 6711236
Messaoud M, Abbes S, Gnaien M, Rebai Y, Kallel A, Jemel S, Cherif G, Skhairia MA, Marouen S, Fakhfekh N (2021) High frequency of Enterocytozoon bieneusi genotype WL12 occurrence among immunocompromised patients with intestinal microsporidiosis. J Fungi 7(3):161. https://doi.org/10.3390/jof7030161
doi: 10.3390/jof7030161
Khanduja S, Ghoshal U, Agarwal V, Pant P, Ghoshal UC (2017) Identification and genotyping of Enterocytozoon bieneusi among human immunodeficiency virus infected patients. J Infect Public Health 10(1):31–40. https://doi.org/10.1016/j.jiph.2016.01.005
doi: 10.1016/j.jiph.2016.01.005
pubmed: 27102928
Liu H, Jiang Z, Yuan Z, Yin J, Wang Z, Yu B, Zhou D, Shen Y, Cao J (2017) Infection by and genotype characteristics of Enterocytozoon bieneusi in HIV/AIDS patients from Guangxi Zhuang autonomous region. China BMC Infect Dis 17(1):1–8. https://doi.org/10.1186/s12879-017-2787-9
doi: 10.1186/s12879-017-2787-9
Saigal K, Khurana S, Sharma A, Sehgal R, Malla N (2013) Comparison of staining techniques and multiplex nested PCR for diagnosis of intestinal microsporidiosis. Diagn Microbiol Infect Dis 77(3):248–249. https://doi.org/10.1016/j.diagmicrobio.2013.07.004
doi: 10.1016/j.diagmicrobio.2013.07.004
pubmed: 23993212
Rubio J, Lanza M, Fuentes I, Soliman R (2014) A novel nested multiplex PCR for the simultaneous detection and differentiation of Cryptosporidium spp., Enterocytozoon bieneusi and Encephalitozoon intestinalis. Parasitol Int 63(5):664–669. https://doi.org/10.1016/j.parint.2014.05.002
doi: 10.1016/j.parint.2014.05.002
pubmed: 24845535
Kemp R, Kluge J (1975) Encephalitozoon sp. in the blue-masked lovebird, Agapornis personata (Reichenow): first confirmed report of microsporidan infection in birds. J Protozool 22(4):489–491. https://doi.org/10.1111/j.1550-7408.1975.tb05214.x
doi: 10.1111/j.1550-7408.1975.tb05214.x
pubmed: 811790
Tavalla M, Mardani-Kateki M, Abdizadeh R, Soltani S, Saki J (2018) Molecular diagnosis of potentially human pathogenic Enterocytozoon bieneusi and Encephalitozoon species in exotic birds in Southwestern Iran. J Infect Public Health 11(2):192–196. https://doi.org/10.1016/j.jiph.2017.07.028
doi: 10.1016/j.jiph.2017.07.028
pubmed: 28869156
Lobo ML, Xiao L, Antunes F, Matos O (2012) Microsporidia as emerging pathogens and the implication for public health: a 10-year study on HIV-positive and-negative patients. Int J Parasitol 42(2):197–205. https://doi.org/10.1016/j.ijpara.2011.12.002
doi: 10.1016/j.ijpara.2011.12.002
pubmed: 22265899
Galván A, Martín Sánchez A, Pérez Valentín M, Henriques-Gil N, Izquierdo F, Fenoy S, Del Aguila C (2011) First cases of microsporidiosis in transplant recipients in Spain and review of the literature. J Clin Microbiol 49(4):1301–1306. https://doi.org/10.1128/JCM.01833-10
doi: 10.1128/JCM.01833-10
pubmed: 21325545
pmcid: 3122787
Nooshadokht M, Sharifi I, Mohammadi MA, Pirestani M, Afgar A, Mahootchi A, Salari S (2017) Intestinal microsporidiosis in Iran: infection in immune-compromised and immunocompetent patients. Curr Med Mycol 3(1):30. https://doi.org/10.18869/acadpub.cmm.3.1.30
doi: 10.18869/acadpub.cmm.3.1.30
pubmed: 29302628
pmcid: 5747587
Ghaderipour M, Khanaliha K, Mohebali M, Shojaee S, Barkhori M, Mirjalali H, Rezaeian M (2017) Emerging intestinal microsporidia infection in general population in Jiroft district, southeastern Iran: a cross-sectional study in 2013–2014. Iran J Public Health 46(12):1697
pubmed: 29259945
pmcid: 5734970
Nkinin SW, Asonganyi T, Didier ES, Kaneshiro ES (2007) Microsporidian infection is prevalent in healthy people in Cameroon. J Clin Microbiol 45(9):2841–2846. https://doi.org/10.1128/JCM.00328-07
doi: 10.1128/JCM.00328-07
pubmed: 17609328
pmcid: 2045255
Pirestani M, Sadraei J, Forouzandeh Moghadam M (2011) Detection and genotyping of human-associated microsporidia in pigeon Columba livia of Tehran in 2010. Pathobiol Res 14(3):15–24
Pirestani M, Sadraei J, Forouzandeh M (2012) Molecular characterization of zoonotic isolates of Enterocytozoon bieneusi in Iran. KAUMS J (FEYZ) 16(1):51–57