The structure of the oropharyngeal genus Candida fungi community in HIVinfected patients

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Abstract

At the present time virtually no data are available about the structure of the genus Candida fungus able to target HIV-infected patients and serve as an etiological factor of candidiasis. The aforementioned shaped the aim of the study: to examine structure of the Candida genus community colonizing the oropharynx in HIV-infected patients with clinical manifestations of oropharyngeal candidiasis. There was conducted a microbiological study of the oropharynx in 31 HIV-infected patients (51.6% males and 48.4% females) with clinical manifestations of oropharyngeal candidiasis treated at Moscow Infectious Clinic No. 2 inpatient department in the years 2015–2017. We confirmed the diversity of the oropharyngeal Candida spp. community found in HIV-infected patients. Total 52 isolates of the genus Candida were isolated. C. albicans dominated in 57.7% cases, whereas C. glabrata prevailed (21.1%) among non-albicans species. Minor components were represented by C. tropicalis (11.5%) and C. krusei (9.6%). C. albicans and C. glabrata were sensitive to polyenes, whereas minor community components — to itroconazole and clotrimazole. The vast majority of fungal strains were resistant to fluconazole. The genus Candida community reveals a unique architecture so that any member may exist in the oropharyngeal biotope of HIV-infected patients as a monoculture or in association: homogeneous, consisting of a single species strains, or heterogeneous, formed by several species. Candida fungi in 18 patients (58.1%) were isolated as a monoculture, whereas in 13 (41.9%) subjects — in association consisting of 34 isolates (65.4% of total number), of which 16 (30.8%) and 18 (34.6%) were isolated from homogeneous and heterogeneous associations, respectively. There were identified 9 two-component associations (69.2%), and 4 (30.8%) consisting of three or more components. It turned out that pattern of the examined community was mainly determined by species composition that agrees with previous data. Most common associations were presented by C. krusei (100%) and C. albicans (73.3%). Upon that, most often C. albicans (72.7%) formed a homogeneous type of associations. Sensitivity of Candida fungi to antimycotic drugs also depended on the architecture of related community. C. albicans isolates in heterogeneous associations revealed a wide range of resistance acquired by contact with non-albicans species.

About the authors

A. D. Voropaev

I.M. Sechenov First Moscow State Medical University

Email: nesviz@mail.ru

PhD Student, Department of Microbiology, Virology and Immunology 

Moscow 

Russian Federation

D. A. Yekaterinchev

I.M. Sechenov First Moscow State Medical University

Email: nesviz@mail.ru

PhD Student, Department of Microbiology, Virology and Immunology

Moscow 

Russian Federation

Yu. V. Nesvizhsky

I.M. Sechenov First Moscow State Medical University

Author for correspondence.
Email: nesviz@mail.ru
ORCID iD: 0000-0003-0386-3883

Yuri V. Nesvizhsky,  PhD, MD (Medicine), Professor, Professor of the Department of Microbiology, Virology and Immunology

119991, Moscow, Trubetskaya str., 8/2

Phone: +7 (916) 889-88-75 

Russian Federation

V. V. Zverev

I.M. Sechenov First Moscow State Medical University

Email: nesviz@mail.ru

RAS Full Member, PhD, MD (Biology), Professor, Head of the Department of Microbiology, Virology and Immunology

Moscow 

Russian Federation

S. S. Afanasiev

Gabrichevsky Institute of Epidemiology and Microbiology

Email: nesviz@mail.ru

PhD, MD (Medicine), Professor, Head Researcher

Moscow 

Russian Federation

E. V. Volchkova

I.M. Sechenov First Moscow State Medical University

Email: nesviz@mail.ru

PhD, MD (Medicine), Professor, Head of the Department of Infectious Diseases

Moscow 

Russian Federation

M. S. Afanasiev

I.M. Sechenov First Moscow State Medical University

Email: nesviz@mail.ru

PhD, MD (Medicine), Professor of the Department of Clinical Allergology and Immunology

Moscow 

Russian Federation

E. V. Budanova

I.M. Sechenov First Moscow State Medical University

Email: nesviz@mail.ru

PhD (Medicine), Associate Professor, Department of Microbiology, Virology and Immunology

Moscow 

Russian Federation

R. E. Boshjan

I.M. Sechenov First Moscow State Medical University

Email: nesviz@mail.ru

PhD (Medicine), Associate Professor, Department of Microbiology, Virology and Immunology

Moscow 

Russian Federation

E. I. Likhanskaya

Gabrichevsky Institute of Epidemiology and Microbiology

Email: nesviz@mail.ru

PhD (Biology), Head of the Laboratory of Microbiology and Prophylaxis of Intestinal Infections

Moscow 

Russian Federation

Y. N. Urban

Gabrichevsky Institute of Epidemiology and Microbiology

Email: fake@neicon.ru

PhD (Biology), Senior Researcher, Laboratory of Clinical Microbiology and Biotechnology

Moscow 

Russian Federation

Yu. S. Filina

The Infectious Hospital No. 2 of the city of Moscow

Email: fake@neicon.ru

PhD (Medicine), Infectologist

Moscow 

Russian Federation

M. E. Suleymanova

I.M. Sechenov First Moscow State Medical University

Email: fake@neicon.ru

Student

Moscow 

Russian Federation

V. A. Voropaeva

I.M. Sechenov First Moscow State Medical University

Email: fake@neicon.ru

Student

Moscow 

Russian Federation

References

  1. Богданова Е.А., Несвижский Ю.В. Архитектоника микробного сообщества желудочно-кишечного тракта // Вестник РАМН. 2010. № 11. С. 38–42. [Bogdanova E.A., Nesvizhsky Yu.V. Architectonics of gastrointestinal microbial community. Vestnik Rossiyskoy akademii meditsinskikh nauk = Annals of the Russian Academy of Medical Sciences, 2010, no. 11, pp. 38–42. (In Russ.)] doi: 10.18821/1560-9529-2017-22-6-311-319
  2. Исследование клинического материала на наличие ДНК возбудителей ИППП и других инфекций органов репродукции методом ПЦР с гибридизационно-флуоресцентной детекцией: методические рекомендации. М.: ФБУН ЦНИИ эпидемиологии Роспотребнадзора, 2006. 138 с. [Examining of clinical material for DNA of sexually transmitted infections and other reproductive organs infections pathogens by hyrbrid fluorometric PCR: methodological recommendations. Мoscow: Central Research Institute of Epidemiology of Rospotrebnadzor, 2006. 138 p. (In Russ.)]
  3. Инструкция по заполнению годовой формы федерального государственного статистического наблюдения № 61 «Сведения о контингентах больных ВИЧ-инфекцией»: приложение к Приказу Министерства здравоохранения и социального развития РФ от 17 марта 2006 г. № 166. [Completion guidelines for the annual federal state statistical survey form No. 61 “Data on HIV-infected patients cohorts”: a supplement for Order No. 166 on 17.03.2006 of the Ministry of Health and Social Development of the Russian Federation. (In Russ.)] URL: https://base.garant.ru/12145892 (15.11.2020)
  4. Урбах В.Ю. Статистический анализ в биологических и медицинских исследованиях. М.: Медицина, 1975. 295 с. [Urbach V.Yu. Statistical analysis in biological and medical research. Мoscow: Medicine, 1975. 295 p. (In Russ.)]
  5. Шевяков М.А. Антибиотик-ассоциированная диарея и кандидоз кишечника: возможности лечения и профилактики // Антибиотики и химиотерапия. 2004. Т. 49, № 10. С. 26–29. [Shevyakov M.A. Antibiotiс-associated diarrhea and candidiasis of an intestine: possibilities of treatment and prophylaxis. Antibiotiki i khimioterapiya = Antibiotics and Chemotherapy, 2004, vol. 49, no. 10, pp. 26–29. (In Russ.)]
  6. Ambe N.F., Longdoh N.A., Tebid P., Bobga T.P., Nkfusai C.N., Ngwa S.B., Nsai F.S., Cumber S.N. The prevalence, risk factors and antifungal sensitivity pattern of oral candidiasis in HIV/AIDS patients in Kumba District Hospital, South West Region, Cameroon. Pan. Afr. Med. J., 2020, vol. 36: 23. doi: 10.11604/pamj.2020.36.23.18202
  7. Awoyeni A., Olaniran O., Odetoyin B., Hassan-Olajokun R., Olopade B., Afolayan D., Adekunle O. Isolation and evaluation of Candida species and their association with CD4+ T cells counts in HIV patients with diarrhea. Afr. Health Sci., 2017, vol. 17, no. 2, pp. 322–329. doi: 10.4314/ahs.v17i2.5
  8. Berkow E.L., Lockhart S.R. Fluconazole resistance in Candida species: a current perspective. Infect. Drug Resist., 2017, no. 10, pp. 237–245. doi: 10.2147/IDR.S118892
  9. Bhattacharya S., Sae-Tia S., Fries B.C. Candidiasis and mechanisms of antifungal resistance. Antibiotics (Basel), 2020, vol. 9, no. 6: 312. doi: 10.3390/antibiotics9060312
  10. Clark-Ordóñez I., Callejas-Negrete O.A., Aréchiga-Carvajal E.T., Mouriño-Pérez R.R. Candida species diversity and antifungal susceptibility patterns in oral samples of HIV/AIDS patients in Baja California, Mexico. Med. Mycol., 2017, vol. 55, no. 3, pp. 285–294. doi: 10.1093/mmy/myw069
  11. Cleveland A.A., Farley M.M., Harrison L.H., Stein B., Hollick R., Lockhart S.R., Magill S.S., Derado G., Park B.J., Chiller T.M. Changes in incidence and antifungal drug resistance in candidemia: results from population-based laboratory surveillance in Atlanta and Baltimore, 2008–2011. Clin. Infect. Dis., 2012, vol. 55, no. 10, pp. 1352–1361. doi: 10.1093/cid/cis697
  12. Cleveland A.A., Harrison L.H., Farley M.M., Hollick R., Stein B., Chiller T.M., Lockhart S.R., Park B.J. Declining incidence of candidemia and the shifting epidemiology of Candida resistance in two US metropolitan areas, 2008–2013: results from population-based surveillance. PLoS One, 2015, vol. 10, no. 3: e0120452. doi: 10.1371/journal.pone.0120452
  13. Enoch D.A., Yang H., Aliyu S.H., Micallef C. The changing epidemiology of invasive fungal infections. Methods Mol. Biol., 2017, no. 1508, pp. 17–65. doi: 10.1007/978-1-4939-6515-1_2
  14. Goulart L.S., Souza W.W.R., Vieira C.A., Lima J.S., Olinda R.A., Araújo C. Oral colonization by Candida species in HIVpositive patients: association and antifungal susceptibility study. Einstein (Sao Paulo), 2018, vol. 16, no. 3: eAO4224. doi: 10.1590/S1679-45082018AO4224
  15. Gow N.A., Brown A.J., Odds F.C. Fungal morphogenesis and host invasion. Curr. Opin. Microbiol., 2002, vol. 5, pp. 366–371. doi: 10.1016/s1369-5274(02)00338-7
  16. Hager C.L., Ghannoum M.A. The mycobiome in HIV. Curr. Opin. HIV AIDS, 2018, vol. 1, no. 13, pp. 69–72. doi: 10.1097/COH.0000000000000432
  17. Jung I.Y., Jeong S.J., Kim Y.K., Kim H.Y., Song Y.G., Kim J.M., Choi J.Y. A multicenter retrospective analysis of the antifungal susceptibility patterns of Candida species and the predictive factors of mortality in South Korean patients with candidemia. Medicine (Baltimore), 2020, vol. 99, no. 11: e19494. doi: 10.1097/MD.0000000000019494
  18. Lamichhane K., Adhikari N., Bastola A., Devkota L., Bhandari P., Dhungel B., Thapa Shrestha U., Adhikari B., Banjara M.R., Rijal K.R., Ghimire P. Biofilm-producing candida species causing oropharyngeal candidiasis in HIV patients attending Sukraraj Tropical and Infectious Diseases Hospital in Kathmandu, Nepal. HIV AIDS (Auckl.), 2020, no. 12, pp. 211–220. doi: 10.2147/HIV.S255698
  19. Olson M.L., Jayaraman A., Kao K.C. Relative ABUNDANCES of Candida albicans and Candida glabrata in in vitro coculture biofilms impact biofilm structure and formation. Appl. Environ. Microbiol., 2018, vol. 84, no. 8: e02769-17. doi: 10.1128/AEM.02769-17
  20. Osaigbovo I.I., Lofor P.V., Oladele R.O. Fluconazole resistance among oral candida isolates from people living with HIV/AIDS in a Nigerian Tertiary Hospital. J. Fungi (Basel), 2017, vol. 3, no. 4: 69. doi: 10.3390/jof3040069
  21. Pfaller M.A., Rhomberg P.R., Messer S.A., Jones R.N., Castanheira M. Isavuconazole, micafungin, and 8 comparator antifungal agents’ susceptibility profiles for common and uncommon opportunistic fungi collected in 2013: temporal analysis of antifungal drug resistance using CLSI species-specific clinical breakpoints and proposed epidemiological cutoff values. Diagn. Microbiol. Infect. Dis., 2015, vol. 82, no. 4, pp. 303–313. doi: 10.1016/j.diagmicrobio.2015.04.008
  22. Spalanzani R.N., Mattos K., Marques L.I., Barros P.F.D., Pereira P.I.P., Paniago A.M.M., Mendes R.P., Chang M.R. Clinical and laboratorial features of oral candidiasis in HIV-positive patients. Rev. Soc. Bras. Med. Trop., 2018, vol. 51, no. 3, pp. 352–356. doi: 10.1590/0037-8682-0241-2017

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Copyright (c) 2020 Voropaev A.D., Yekaterinchev D.A., Nesvizhsky Y.V., Zverev V.V., Afanasiev S.S., Volchkova E.V., Afanasiev M.S., Budanova E.V., Boshjan R.E., Likhanskaya E.I., Urban Y.N., Filina Y.S., Suleymanova M.E., Voropaeva V.A.

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