Frequency of Candida species in the oral cavity of narcotics and stimulants smokers in Isfahan, using polymerase chain reaction-restriction fragment length polymorphism method

Document Type : Original Article


1 Department of Parasitology and Mycology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran

2 Department of Cognitive Rehabilitation, Brain and Cognition Clinic, Institute for Cognitive Science Studies, Tehran, Iran

3 Department of Laboratory Sciences, School of Paramedical Sciences, Torbat Heydariyeh University of Medical Sciences, Torbat; Health Sciences Research Center, Torbat Heydariyeh University of Medical Sciences, Torbat Heydariyeh, Iran


Background: Candida species are a group of coexistent microorganisms in the oral cavity that opportunistically cause disease in vulnerable people, including addicts. This study is aimed at identifying and determining the frequency of Candida species in the oral cavity of the addicts to inform the epidemiological panel and to warn to prevent the resistance of the species. Materials and Methods: In this study, sampling was done from the oral cavity of 83 addicts who referred to Addiction Treatment Centers in Isfahan, Iran, using moist sterile swab. The presence of yeast on the direct microscope slides of 58 samples was confirmed. To carry out culture and the primary identification, Sabouraud dextrose agar medium with chloramphenicol as well as HiCrome Candida agar medium was used. Isolates were identified by polymerase chain reaction (PCR) restriction fragment length polymorphism (using specific primers ITS1-ITS4 and MSP I enzyme) and Duplex PCR test (using specific primers CDU1-CDU2/CAL1-CAL2). Results: Out of 93 Candida isolates which had been isolated from 58 culture-positive samples of the oral cavity, Candida albicans (41.93%) were the most prevalent species, followed by Candida dubliniensis (24.73%), Candida glabrata (21.50%), Candida kefyr (8.60%), Candida tropicalis (2.15%), and Candida parapsilosis (1.07%), respectively. In 33 cases (56.90%), the presence of more than one Candida species was observed. Conclusion: Compared to the studies conducted on the oral cavity of healthy controls, smoking certain drugs can have a significant effect on the presence and frequency of Candida species, particularly C. dubliniensis and C. glabrata.


Anaissie E, McGinnis M, Pfaller M. Clinical Mycology. Churchill Livingstone: London, UK: Elsevier Health Sciences; 2009.  Back to cited text no. 1
Ranjan K, Poças-Fonseca MJ. Genetic diversity of pathogenic yeasts. In: Microbial Diversity in Ecosystem Sustainability and Biotechnological Applications. Singapore: Springer; 2019. p. 593-615.  Back to cited text no. 2
AL-Janabi AA, Al-Mosawe HA, Karrar AM. Yeasts: One member of the normal flora of the oral cavity. Int J Med Sci Curr Res 2019;2:345.  Back to cited text no. 3
Theill L, Dudiuk C, Morano S, Gamarra S, Nardin ME, Méndez E, et al. Prevalence and antifungal susceptibility of Candida albicans and its related species Candida dubliniensis and Candida africana isolated from vulvovaginal samples in a hospital of Argentina. Rev Argent Microbiol 2016;48:43-9.  Back to cited text no. 4
Vázquez-González D, Perusquía-Ortiz AM, Hundeiker M, Bonifaz A. Opportunistic yeast infections: Candidiasis, cryptococcosis, trichosporonosis and geotrichosis. J Dtsch Dermatol Ges 2013;11:381-93.  Back to cited text no. 5
Polvi EJ, Li X, O'Meara TR, Leach MD, Cowen LE. Opportunistic yeast pathogens: Reservoirs, virulence mechanisms, and therapeutic strategies. Cell Mol Life Sci 2015;72:2261-87.  Back to cited text no. 6
Mobeen N. Oral candidiasis – A short review. Int J Curr Res Rev 2014;6:89.  Back to cited text no. 7
Vila T, Sultan AS, Montelongo-Jauregui D, Jabra-Rizk MA. Oral candidiasis: A disease of opportunity. J Fungi (Basel) 2020;6(1):15.  Back to cited text no. 8
Leen CL, Brettle RP. Fungal infections in drug users. J Antimicrob Chemother 1991;28 Suppl A: 83-96.  Back to cited text no. 9
Valadas LAR, Fernandes ML, Silva MI, Citó C, Maia IC, de Carvalho MR, et al. Oral manifestations of drug abuse: A review of literature. J Young Pharm 2020;12:483.  Back to cited text no. 10
Hser YI, Hoffman V, Grella CE, Anglin MD. A 33-year follow-up of narcotics addicts. Arch Gen Psychiatry 2001;58:503-8.  Back to cited text no. 11
MacLeod CM. The stroop task: The gold standard of attentional measures. J Exp Psychol Gen 1992;121:12-4.  Back to cited text no. 12
Shelby CL. Addiction and Meaning Addiction. Palgrave Macmillan, London: Springer; 2016. p. 101-21.  Back to cited text no. 13
Association American Psychiatric. Diagnostic and Statistical Manual of Mental Disorders (DSM-5®). Washington, DC, USA: American Psychiatric Publishing; 2013.  Back to cited text no. 14
Brown SA, Myers MG, Lippke L, Tapert SF, Stewart DG, Vik PW. Psychometric evaluation of the customary drinking and drug use record (CDDR): A measure of adolescent alcohol and drug involvement. J Stud Alcohol 1998;59:427-38.  Back to cited text no. 15
Hussey HH, Katz S. Infections resulting from narcotic addiction; report of 102 cases. Am J Med 1950;9:186-93.  Back to cited text no. 16
Lo TW, Yeung JW, Tam CH. Substance abuse and public health: A multilevel perspective and multiple responses. Int J Environ Res Public Health 2020;17:2610.  Back to cited text no. 17
Sapira JD. The narcotic addict as a medical patient. Am J Med 1968;45:555-88.  Back to cited text no. 18
Friedman H, Pross S, Klein TW. Addictive drugs and their relationship with infectious diseases. FEMS Immunol Med Microbiol 2006;47:330-42.  Back to cited text no. 19
Nucci M, Marr KA. Emerging fungal diseases. Clin Infect Dis 2005;41:521-6.  Back to cited text no. 20
Moyano J, Aguirre L. Opioids in the immune system: From experimental studies to clinical practice. Rev Assoc Méd Bras 2019;65:262-9.  Back to cited text no. 21
Farah CS, Lynch N, McCullough MJ. Oral fungal infections: An update for the general practitioner. Aust Dent J 2010;55 Suppl 1:48-54.  Back to cited text no. 22
Goel D, Patthi B, Singla A, Malhi R, Chaudhary PK, Khan A. Assessment of knowledge and attitude regarding management of patients with substance usage in dental clinics in Modinagar – A cross-sectional study. J Family Med Prim Care 2019;8:3683-8.  Back to cited text no. 23
[PUBMED]  [Full text]  
Keboa MT, Enriquez N, Martel M, Nicolau B, Macdonald ME. Oral health implications of cannabis smoking: A rapid evidence review. J Can Dent Assoc 2020;86:k2.  Back to cited text no. 24
Abharian PH, Dehghan P, Abharian PH, Tolouei S. Molecular characterization of Candida dubliniensis and Candida albicans in the oral cavity of drug abusers using duplex polymerase chain reaction. Curr Med Mycol 2018;4:12-7.  Back to cited text no. 25
Li X, Kolltveit KM, Tronstad L, Olsen I. Systemic diseases caused by oral infection. Clin Microbiol Rev 2000;13:547-58.  Back to cited text no. 26
Nacher M, Adenis A, Hanf M, Adriouch L, Vantilcke V, El Guedj M, et al. Crack cocaine use increases the incidence of AIDS-defining events in French Guiana. AIDS 2009;23:2223-6.  Back to cited text no. 27
Freire-Garabal M, Núñez MJ, Balboa J, Rodríguez-Cobo A, López-Paz JM, Rey-Méndez M, et al. Effects of amphetamine on development of oral candidiasis in rats. Clin Diagn Lab Immunol 1999;6:530-3.  Back to cited text no. 28
Maheronnaghsh M, Tolouei S, Dehghan P, Chadeganipour M, Yazdi M. Identification of Candida species in patients with oral lesion undergoing chemotherapy along with minimum inhibitory concentration to fluconazole. Adv Biomed Res 2016;5:132.  Back to cited text no. 29
[PUBMED]  [Full text]  
Fidel PL, Vazquez JA, Sobel JD. Candida glabrata: Review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans. Clin Microbiol Rev 1999;12:80-96.  Back to cited text no. 30
Golirad N, Fozouni L, Pordeli H. Evaluation of susceptibility to fluconazole and voriconazole in oral Candida glabrata isolates from drug addicts. Int J High Risk Behav Addict. 2019; 8 (4):e92807.  Back to cited text no. 31
Ramani R, Chaturvedi V. Flow cytometry antifungal susceptibility testing of pathogenic yeasts other than Candida albicans and comparison with the NCCLS broth microdilution test. Antimicrob Agents Chemother 2000;44:2752-8.  Back to cited text no. 32
Yang YL, Li SY, Cheng HH, Lo HJ; TSARY Hospitals. The trend of susceptibilities to amphotericin B and fluconazole of Candida species from 1999 to 2002 in Taiwan. BMC Infect Dis 2005;5:99.  Back to cited text no. 33
Silva GA, Bernardi TL, Schaker PD, Menegotto M, Valente P. Rapid yeast DNA extraction by boiling and freeze-thawing without using chemical reagents and DNA purification. Braz Arch Biol Technol 2012;55:319-27.  Back to cited text no. 34
Mirhendi H, Makimura K, Khoramizadeh M, Yamaguchi H. A one-enzyme PCR-RFLP assay for identification of six medically important Candida species. Nihon Ishinkin Gakkai Zasshi 2006;47:225-9.  Back to cited text no. 35
Majima T, Ito-Kuwa S, Nagatomi R, Nakamura K. Study of the oral carriage of Candida sp. in dental students and staff – Identification of Candida sp. and background survey. Oral Sci Int 2014;11:30-4.  Back to cited text no. 36
Mohammadi R, Mirhendi H, Rezaei-Matehkolaei A, Ghahri M, Shidfar MR, Jalalizand N, et al. Molecular identification and distribution profile of Candida species isolated from Iranian patients. Med Mycol 2013;51:657-63.  Back to cited text no. 37
Gutiérrez J, Morales P, González MA, Quindós G. Candida dubliniensis, a new fungal pathogen. J Basic Microbiol 2002;42:207-27.  Back to cited text no. 38
Hadzic S, Dedic A, Gojkov-Vukelic M, Mehic-Basara N, Hukic M, Babic M, et al. The effect of psychoactive substances (drugs) on the presence and frequency of oral Candida species and Candida dubliniensis. Mater Sociomed 2013;25:223-5.  Back to cited text no. 39
Mokri A. Brief overview of the status of drug abuse in Iran. Arch Iranian Med 2002;5:184-90.  Back to cited text no. 40
Mokeem SA, Abduljabbar T, Al-Kheraif AA, Alasqah MN, Michelogiannakis D, Samaranayake LP, et al. Oral Candida carriage among cigarette- and waterpipe-smokers, and electronic cigarette users. Oral Dis 2019;25:319-26.  Back to cited text no. 41
Javaheri M, Mohammadi F, Chadeganipour M, Nekoian S, Dehghan P. Identification of Candida species in oral cavity of smokers and nonsmokers. J Isfahan Med School 2015;33:2105-10.  Back to cited text no. 42
Heidarian A, Dehghan P, Chadeganipour M, Tayeri K. Frequency of Candida species isolated from the oral cavity of HIV-infected patients referring to behavioral disease counseling center of Isfahan in 2017-2018. SJKU 2019;24:30-41.  Back to cited text no. 43
Maheshwari M, Kaur R, Chadha S. Candida species prevalence profile in HIV seropositive patients from a major tertiary care hospital in New Delhi, India. J Pathog 2016;2016:1-8.  Back to cited text no. 44
Dronda F, Alonso-Sanz M, Laguna F, Chaves F, Martínez-Suárez JV, Rodríguez-Tudela JL, et al. Mixed oropharyngeal candidiasis due to Candida albicans and non-albicans Candida strains in HIV-infected patients. Eur J Clin Microbiol Infect Dis 1996;15:446-52.  Back to cited text no. 45
Friedman H, Newton C, Klein TW. Microbial infections, immunomodulation, and drugs of abuse. Clin Microbiol Rev 2003;16:209-19.  Back to cited text no. 46
Yu Q, Zhang D, Walston M, Zhang J, Liu Y, Watson RR. Chronic methamphetamine exposure alters immune function in normal and retrovirus-infected mice. Int Immunopharmacol 2002;2:951-62.  Back to cited text no. 47
Anwar KP, Malik A, Subhan KH. Profile of candidiasis in HIV infected patients. Iran J Microbiol 2012;4:204-9.  Back to cited text no. 48
Irwin MR, Olmos L, Wang M, Valladares EM, Motivala SJ, Fong T, et al. Cocaine dependence and acute cocaine induce decreases of monocyte proinflammatory cytokine expression across the diurnal period: Autonomic mechanisms. J Pharmacol Exp Ther 2007;320:507-15.  Back to cited text no. 49
Katiraee F, Khosravi AR, Khalaj V, Hajiabdolbaghi M, Khaksar AA, Rasoulinejad M, et al. Oral candidiasis in human immunodeficiency virus (HIV) infected individuals in Iran. Tehran Univ Med J 2010;68:37-44.  Back to cited text no. 50
Vivancos-Gallego MJ, Okhai H, Perez-Elías MJ, Gomez-Ayerbe C, Moreno-Zamora A, Casado JL, et al. CD4+:CD8+ T-cell ratio changes in people with HIV receiving antiretroviral treatment. Antivir Ther. 2020;10.3851/IMP3354. [published online ahead of print, 2020 Apr 27].  Back to cited text no. 51