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Thank you for visiting nature. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser or turn off compatibility mode in Internet Explorer. In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript. Yeast species are a group of coexistent microorganisms in the oral cavity that can cause opportunistic infections in vulnerable individuals, including addicts. This study aimed to identify the yeast species profile responsible for oral yeast colonization OYC and the associated risk factors in patients with substance use disorder SUD in Ahvaz, Iran. Oral samples were collected from drug users hospitalized in 12 addiction treatment centers, and the related clinical information was mined. A total of yeast strains were identified from individuals with substance abuse. Candida albicans was the most common species Moreover, uncommon oral yeasts constituted 5. Importantly, OYC exhibited associations with such factors as duration of drug use, daily drug consumption rate, opioid utilization, oral drug administration, and the Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition DSM-5 score. The present study is the pioneering investigation revealing the prevalence and diversity of oral yeast species, along with associated risk factors, in individuals with SUD in southwestern Iran. Furthermore, it underscores the importance of developing efficient and cost-effective diagnostic methods tailored for resource-constrained settings. The incidence of oral fungal infections has increased over the past few decades, which can cause symptoms ranging from mild oral disease to severe systemic infections, particularly in immunocompromised individuals 1. Although the majority of yeast species isolated from the oral cavity are due to Candida albicans , infections due to non- albicans Candida NAC species, including those with resistance to azole antifungals, are progressively on the rise 2 , 3. This shift in the prevalence of C. In addition, there has been a recent surge in reported cases of infections caused by uncommon yeast species such as Trichosporon , Rhodotorula , Geotrichum , Pichia , and Saccharomyces spp. Several underlying factors contribute to the development of oral yeast infections, including diabetes, immunodeficiency syndrome, soft tissue injury, loss of natural defensive barriers, use of artificial teeth, and addiction 7. Addiction is a persistent condition characterized by the compulsive use of drugs despite negative consequences, which presents a major threat to both individuals and societies. Today, addiction is considered as a major public health concern due to its association with a range of adverse health outcomes and infections 8. People with substance use disorders SUD are more vulnerable to oral yeast infections due to factors such as compromised oral hygiene, immunosuppression, malnutrition, and interactions between substances and oral microorganisms 9 , In addicted individuals, particularly those with compromised immune systems, these factors can not only harm mucosal immune defenses but also disrupt the physiological and microbial ecology of the oral environment. This can lead to chronic dry mouth and reduced salivation, which promote the colonization of yeast species in the mouth. Consequently, systemic infections associated with significant morbidity and mortality rates may occur Traditionally, the widely available methods for identifying yeast species in clinical laboratories are phenotypic and biochemical assays, but these methods can be labor-intensive, time-consuming, and prone to errors, particularly for unusual yeast species Although ribosomal DNA sequencing is considered to be the gold standard technique for the identification of yeast species, this technique is expensive and thus not widely utilized in routine laboratories On the other hand, there are only a few polymerase chain reaction PCR based techniques available that can accurately target a comprehensive list of opportunistic yeast species Recently, the multiplex PCR assay has proven to be a successful rapid technique for identifying opportunistic yeast species. Since utilizing the plex PCR test to identify common and unusual yeasts can decrease processing times and expenses, this approach could be helpful for use in developing countries. Accordingly, this study was conducted to explore the prevalence and diversity of oral yeast species among individuals with SUD in Ahvaz, southwestern Iran. The innovative use of the plex PCR technique expedites yeast species identification and provides a cost-effective alternative, especially in resource-constrained settings. The research can significantly enhance our understanding of oral Candida spp. Moreover, the findings can help identify key risk factors, including demographic characteristics and drug-related factors, contributing to oral yeast colonization OYC. The outcomes might offer valuable insights for effective management and appropriate intervention strategies in this vulnerable population. This study included a total of participants males and 62 females hospitalized in 12 addiction treatment centers in Ahvaz, southwestern Iran. All participants were included in the study after signing an informed consent form prior to inclusion in the study. Oral samples were collected between 27 December, and 19 July, The inclusion criteria were as follows: being drug addicts receiving inpatient care at addiction treatment centers, providing an informed consent to participate in the study, and having medical records available at the centers. Sampling of the internal surfaces of the entire oral cavity was performed using a sterile cotton swab. Afterwards, the yeasts were differentiated according to the morphology and color of their colonies, and the number of colonies was counted based on their colony forming units CFUs per swab. The yeast isolates obtained from the chromogenic medium were subsequently transferred into two sets of microtubes each filled with sterile distilled water. The microtubes served as long-term sources for the isolates and were kept under both room temperature and refrigerated condition. The yeast isolates were subcultured on Sabouraud dextrose agar Lifoilchem, Roseto degli Abruzzi, Italy containing chloramphenicol for 48 h. To initiate DNA extraction, one full loop of the freshly grown yeast colonies was transferred into 2 ml screw cap tubes. After vortexing the suspensions for 2 min, they were centrifuged for 5 min at 10, rpm. The resulting supernatant was then carefully transferred to a new 1. This was followed by centrifugation at 12, rpm for 15 min. The yield and purity of the extracted DNA were assessed using a nanophotometer by measuring the absorbance at nm and nm. The identification of yeasts was carried out using the plex PCR method, following a protocol outlined by Arastehfar et al. This technique includes three multiplex PCR reactions, with the first identifying the most common Candida species, the second targeting uncommon Candida species, and the third multiplex test identifying the most clinically significant basidiomycete yeasts like Geotrichum , Trichosporon , Cryptococcus , and Rhodotorula. Bidirectional chain Terminated Sanger sequencing using referenced primers were performed. The species of each isolate was assigned based on the sequence with the highest similarity, and then the results were deposited to the GenBank. Moreover, the independent t-test was employed to compare the means of quantitative variables between the two groups of patients with OYC versus without OYC. Further analysis was performed using multiple logistic regression MLR model to investigate the factors associated with having OYC among the subjects. In addition, we compared the overall discriminative capacity of the variables regarding OYC by using the area under the receiver operating characteristic curve AUC. All analysis was performed in the SPSS v. In total, we diagnosed strains of yeasts and yeast-like fungi from substance abusers Table 1. The most common species among the NAC isolates were C. In this study, 5. The data also demonstrated that more than one Candida spp. The most common co-colonization was a combination of C. Figure 1 compares the number of colonies between C. The results of the chi-square test indicated a statistically significant difference in the frequency distribution of colony counts between C. Our data also showed that yeast isolates This technique successfully identified all Candida species, as well as certain rare yeast species such as C. The remaining eight unknown isolates were subsequently identified and confirmed at the species level using rDNA sequencing, revealing the presence of S. Electrophoretic pattern of plex PCR products. Numbers 1 to 13 encompass the following: negative control, Candida tropicalis, Candida glabrata, Candida parapsilosis, Candida albicans, Candida dubliniensis , pichia kudriavzevii Candida krusei , Marker , Clavispora lusitaniae Candida lusitaniae , Kluyveromyces marxianus Candida kefyr , Marker , Geotrichum candidum, and Trichosporon asahii. Out of the drug abusers included in the study, patients The demographic characteristics of patients are summarized in Table 3. The mean age of the patients with and without OYC was Among the infected patients, 50 The majority of OYC cases were observed in individuals with underlying diseases Although the prevalence of OYC was greater among cigarette users Table 4 presents the relationship between the consumption methods and the type of drugs with the occurrence of OYC. Based on the findings, the highest prevalence rates of OYC were related to injection We also observed that OYC was most frequently observed in individuals who used stimulants Furthermore, substance use variables associated with different consumption methods such as oral, injection, and smoking exhibited similar predictive power for characterizing OYC Fig. The factors associated with colonization were subjected to MLR analysis. According to the results, duration of drug use OR: 1. Substance use disorders are associated with numerous medical, psychiatric, and economic problems, creating a significant burden for affected individuals and society To date, limited studies have investigated the prevalence of yeast species and the related factors in addicted individuals. To address this gap, we conducted this study in southwestern Iran and identified a noteworthy rate of OYC Similarly, a study conducted in northeast Iran examined 83 oral samples from individuals with addiction and detected oral candidiasis in In another study conducted in central Iran, PCR results from oral samples showed a high frequency In a recent study by Navabi et al. Conversely, Khalili et al. In another study conducted in Spain, Sheth et al. The microbiological analysis conducted by Hadzic et al. This variation might be due to differences in geographical locations, certain characteristics of the individuals such as age, oral hygiene, or the presence of dentures , different sample collection methods, and diverging identification techniques. Our data concur with our previous findings that addiction may be a contributing factor to the high occurrence of yeast species in the oral cavity. The current evidence indicates that addiction can lead to a compromised local and systemic immune system, thereby creating a conducive environment for pathogen acquisition and the development of oral yeasts 24 , Opiates, for instance, can directly impact the immune system by binding to opioid receptors on immune cells, resulting in reduced phagocytosis and chemotaxis On the other hand, opium addiction significantly disrupts the cytokine network, creating a conducive environment for fungal infections 9 , Furthermore, drug-induced vasoconstriction and reduced saliva production in individuals with addiction can elevate the increase of OYC in the oral cavity Poor oral and dental hygiene, communal living in drug addiction camps, and low economic and cultural status are important contributing factors associated with an increased risk of OYC in this population It should be noted that diagnostic techniques may also impact the prevalence of yeast species. In this study, the combination of plex PCR and rDNA sequencing proved to be a powerful technique for accurately identifying yeasts species from the oral cavity. In a previous Iranian study that evaluated candidemia in pediatric patients, We diagnosed species of yeasts and yeast-like fungi from substance abusers in this research. The most frequently isolated yeast species included C. It is worth noting that, consistent with our findings, C. In the past, C. However, accurate differentiation between the two species can now be achieved through the implementation of precise molecular methods The cause for the heightened prevalence of this species in drug-affected patients remains a matter of debate. Hadzic et al. According to these findings, psychoactive substances opiates and alcohol can lead to an increase in oral Candida dubliniensis regardless of the type of addiction Additionally, recent studies suggest that the rise in NAC species may be associated with factors such as immune system status, age, antifungal drug resistance, healthcare facilities, broad-spectrum antibacterial agents, and geography 3 , Interestingly, we found that This difference in results could be attributed to the techniques employed in our study and the favorable oral cavity conditions in individuals with addiction disorders that promote yeast growth. In our investigation, uncommon yeast species accounted for 5. For unidentified isolates, including S. It seems that the exact factors contributing to the emergence of rare yeast species are still unclear. However, sociodemographic variables, the impact of drugs in fostering favorable environments for yeast growth, compromised health status, and the employed identification techniques may contribute to the detection of uncommon yeasts. Importantly, unlike the studies conducted by Maheronnaghsh et al. Among the rare species identified in the present study, G. Moreover, our study reported the first case of an M. In essence, there is serious concern for immunocompromised patients, given that rare yeast isolates possess the potential to infiltrate deeper tissues and induce infections under specific conditions. The present study also revealed significant difference in the occurrence of OYC between females This finding diverges from the results of Suryana et al. The higher occurrence of OYC in women may be attributed to various factors. Hormonal fluctuations, especially during menstruation, pregnancy, or menopause, can affect the oral environment and promote yeast growth. Additionally, the use of hormonal contraceptives may influence the oral microbiota 38 , 39 , In our study, we witnessed that older age was a contributing factor to the development of OYC in individuals with SUD. All individuals aged 50 years or older exhibited colonization in contrast to Old age may be a predisposing factor for oral candidiasis, possibly due to complex systemic conditions, decreased salivary flow, increased medication intake, and denture wearing We did not detect significant differences in the prevalence of OYC between individuals who smoked cigarettes and those who did not smoke cigarettes. However, owing to the limited number of non-cigarette users included in our study, we were unable to conclusively determine whether cigarette smoking influenced the pattern of yeast colonization in the oral cavity. In the present study, we performed a logistic regression analysis to identify the factors associated with oral yeast candidiasis in individuals with substance abuse. Initially, a univariate logistic regression model was fitted, and variables with P-values less than 0. Our analyses revealed that opioid use, oral drug use, rate of drug consumption per day, duration of drug use, and DSM-5 score were significantly associated with the occurrence of OYC. It is worth noting that drugs can be broadly classified into four main groups: opioids tramadol, crack, heroin, opium, methadone, norjizak, and sorche , hallucinogens hashish, grass, marijuana, and mushrooms , stimulants methamphetamine, crystal, and cocaine , and other substances nasvay and alcohol. To our surprise, after controlling for the effect of other variables in the model, the odds of having OYC were 3. Several studies have demonstrated that opioids have suppressive effects on the immune system, which can impact cytokine production, antibody production, and immune cell migration and function 9 , 42 , In addition, chronic drug use could potentially cause structural changes to the oral mucosa and tissues, rendering them more susceptible to fungal overgrowth and colonization 44 , As our results indicated, drug use was observed via various routes, including oral ingestion, injection, and smoking. The results demonstrated that individuals who reported oral drug use had 6. Saliva contains antibodies and enzymes that help control yeasts levels 46 , Furthermore, the results of our study revealed a significant association between longer duration of drug use and higher daily consumption rates with increased odds of OYC. There are various factors that may contribute to this association. Firstly, chronic drug exposure may induce immunosuppression, which can increase the susceptibility to OYC. Secondly, long-term drug use may increase the likelihood of oral side effects, such as xerostomia, which can disrupt the natural defenses of the oral cavity against OYC. Finally, higher cumulative drug intake may lead to a greater disturbance of the oral microbiome, which can promote the growth of Candida spp. One possible explanation is that patients with severe SUD may be less compliant with oral hygiene routines due to their addiction, which could increase their risk of developing OYC. Additionally, individuals with more entrenched addictions may spend less time focusing on oral health symptoms, leading to underreporting of OYC in the study. Nevertheless, further research is imperative to validate these explanations and unveil the underlying mechanisms of this association. The present study revealed a heightened prevalence of oral yeasts, notably uncommon yeast species, in individuals with substance use disorders. Additionally, factors such as the duration of drug use, daily drug consumption, DSM-5 score, opioid use, and oral drug administration were significantly associated with an elevated likelihood of oral yeast colonization. These findings highlight the multifaceted etiology, primarily influenced by drug-related factors that compromise immunity and impact saliva flow and composition. For a more comprehensive understanding of the oral yeast diversity in this high-risk population, it is recommended to carry out further prospective multicenter studies in different geographical regions through employing reliable diagnostic methods. The data that supports the findings of this study are available in the supplementary material of this article. Leaw, S. Identification of medically important yeast species by sequence analysis of the internal transcribed spacer regions. Maheronnaghsh, M. Identification of Candida species in patients with oral lesion undergoing chemotherapy along with minimum inhibitory concentration to fluconazole. Ghojoghi, A. Non-albicans candidemia in cancer patients as an increasing health problem: A comprehensive review and meta-analysis. Asian Pac. Article Google Scholar. Ejdys, E. Biodiversity of mycocoenoses of oral cavity, throat and nose of children aged 6—15 years. PubMed Google Scholar. Species diversity of yeast in oral colonization of insulin-treated diabetes mellitus patients. Article PubMed Google Scholar. Aslani, N. Vila, T. Oral candidiasis: A disease of opportunity. Valadas, L. Oral manifestations of drug abuse: A review of literature. Ayatollahi-Mousavi, S. The effects of opium addiction on the immune system function in patients with fungal infection. Zhang, J. The effects of drug addiction and detoxification on the human oral microbiota. Google Scholar. Guo, F. Invasive candidiasis in intensive care units in China: A multicentre prospective observational study. Arastehfar, A. Ahmed, A. Invasive candidiasis in non neutropenic critically ill-need for region-specific management guidelines. Aboualigalehdari, E. Erfaninejad, M. Epidemiology, prevalence, and associated factors of oral candidiasis in HIV patients from southwest Iran in post-highly active antiretroviral therapy era. Abharian, P. Frequency of Candida species in the oral cavity of narcotics and stimulants smokers in Isfahan, using polymerase chain reaction-restriction fragment length polymorphism method. Patel, V. Addressing the burden of mental, neurological, and substance use disorders: Key messages from disease control priorities. Golirad, N. Evaluation of susceptibility to fluconazole and voriconazole in oral Candida glabrata isolates from drug addicts. Navabi, N. A comparison of the prevalence rate of oral Candida colonization between Opium users and cigarette smokers in Kerman, Iran. Khalili, P. Oral candidiasis and cigarette, tobacco, alcohol, and opium consumption in Rafsanjan, a region in the southeast of Iran. Sheth, C. Alcohol and tobacco consumption affect the oral carriage of Candida albicans and mutans streptococci. Hadzic, S. The effect of psychoactive substances drugs on the presence and frequency of oral Candida species and Candida dubliniensis. Plein, L. Opioids and the immune system—friend or foe. Liang, X. Opioid system modulates the immune function: A review. Kaushik, K. Shooting up: The interface of microbial infections and drug abuse. Suryana, K. Mateos-Moreno, M. Dental profile of a community of recovering drug addicts: Biomedical aspects. Retrospective cohort study. Mirhendi, H. Species distribution and antifungal susceptibility profile of Candida isolates from blood and other normally sterile foci from pediatric ICU patients in Tehran, Iran. Kord, M. Epidemiology of yeast species causing bloodstream infection in Tehran, Iran — ; superiority of plex PCR over the Vitek 2 system for yeast identification. Molecular characterization of Candida dubliniensis and Candida albicans in the oral cavity of drug abusers using duplex polymerase chain reaction. Deepa, A. Uncommon opportunistic fungal infections of oral cavity: A review. Jobbins, J. Oral carriage of yeasts, coliforms and staphylococci in patients with advanced malignant disease. Davies, A. Oral yeast carriage in patients with advanced cancer. Identification of Candida species and antifungal susceptibility in cancer patients with oral lesions in Ahvaz, Southern West of Iran. Hattori, H. A case of oral geotrichosis caused by Geotrichum capitatum in an old patient. Viudes, A. Two cases of fungemia due to Candida lusitaniae and a literature review. Hu, L. Characterization of oral candidiasis and the Candida species profile in patients with oral mucosal diseases. Omosigho, O. Deeiam, K. Presence of Candida and its associated factors in participants attending oral cancer screening in the lower northeastern area of Thailand. Rao, P. Oral candidiasis—A review. Moyano, J. Opioids in the immune system: From experimental studies to clinical practice. Diasso, P. The effects of long-term opioid treatment on the immune system in chronic non-cancer pain patients: A systematic review. Pain 24 , — Shekarchizadeh, H. Oral health status and its determinants among opiate dependents: A cross-sectional study. BMC Oral. Melo, C. Oral changes in cocaine abusers: An integrative review. Mercadante, S. Methadone as a first-line opioid in cancer pain management: A systematic review. Sugimoto, J. Relationship between salivary histatin 5 levels and Candida CFU counts in healthy elderly. Parvaei, P. Investigating the relationship between stimulated salivary markers and the history of opioid use: A case-control study. Hasin, D. DSM-5 criteria for substance use disorders: Recommendations and rationale. Kopak, A. The elimination of abuse and dependence in DSM-5 substance use disorders: What does this mean for treatment?. Download references. We express our thanks to all participants, as well as the staff and authorities of the Addiction Treatment Centers, collaborating with this project. You can also search for this author in PubMed Google Scholar. All authors contributed to the revision. Correspondence to Mahnaz Fatahinia. Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. Reprints and permissions. Exploring the diversity of uncommon oral yeast species and associated risk factors among substance abusers in southwestern Iran. Sci Rep 14 , Download citation. Received : 08 September Accepted : 13 January Published : 22 January Anyone you share the following link with will be able to read this content:. Sorry, a shareable link is not currently available for this article. Provided by the Springer Nature SharedIt content-sharing initiative. Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly. Skip to main content Thank you for visiting nature. Download PDF. Subjects Fungi Microbiology. Abstract Yeast species are a group of coexistent microorganisms in the oral cavity that can cause opportunistic infections in vulnerable individuals, including addicts. Oral microbiome dysbiosis among cigarette smokers and smokeless tobacco users compared to non-users Article Open access 06 May Comparative analysis of the distribution and antifungal susceptibility of yeast species in cat facial hair and human nails Article Open access 26 June Altered oral microbiota and immune dysfunction in Chinese elderly patients with schizophrenia: a cross-sectional study Article Open access 09 December Introduction The incidence of oral fungal infections has increased over the past few decades, which can cause symptoms ranging from mild oral disease to severe systemic infections, particularly in immunocompromised individuals 1. Materials and methods Study design and patient characteristics This study included a total of participants males and 62 females hospitalized in 12 addiction treatment centers in Ahvaz, southwestern Iran. Initial identification of yeasts Sampling of the internal surfaces of the entire oral cavity was performed using a sterile cotton swab. DNA extraction The yeast isolates were subcultured on Sabouraud dextrose agar Lifoilchem, Roseto degli Abruzzi, Italy containing chloramphenicol for 48 h. Molecular assays The identification of yeasts was carried out using the plex PCR method, following a protocol outlined by Arastehfar et al. Results Distribution of yeast species causing OYC In total, we diagnosed strains of yeasts and yeast-like fungi from substance abusers Table 1. Full size table. Table 2 Distribution of co-colonization with different yeast species in patients with OYC. Figure 1. Full size image. Figure 2. Table 3 Comparison of the frequency of socio-demographic characteristics between patients with and without OYC. Table 4 Evaluating the association between methods of drug consumption and type of drug with occurrence of OYC. Figure 3. Table 5 Determining the factors associated with OYC among addicted patients using multiple logistic regression model. Figure 4. Discussion Substance use disorders are associated with numerous medical, psychiatric, and economic problems, creating a significant burden for affected individuals and society Conclusion The present study revealed a heightened prevalence of oral yeasts, notably uncommon yeast species, in individuals with substance use disorders. Data availability The data that supports the findings of this study are available in the supplementary material of this article. References Leaw, S. Article Google Scholar Ejdys, E. Article Google Scholar Vila, T. Google Scholar Guo, F. Google Scholar Patel, V. Article Google Scholar Navabi, N. Article Google Scholar Sheth, C. Article Google Scholar Mirhendi, H. Article Google Scholar Deepa, A. Google Scholar Hattori, H. Google Scholar Deeiam, K. Article Google Scholar Melo, C. Article Google Scholar Sugimoto, J. Article Google Scholar Hasin, D. Article Google Scholar Download references. Acknowledgements We express our thanks to all participants, as well as the staff and authorities of the Addiction Treatment Centers, collaborating with this project. View author publications. Ethics declarations Competing interests The authors declare no competing interests. Additional information Publisher's note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Supplementary Information. Supplementary Figures. About this article. Cite this article Ghojoghi, A. Copy to clipboard. Publish with us For authors Language editing services Submit manuscript. Search Search articles by subject, keyword or author. Show results from All journals This journal. Advanced search. Close banner Close. Email address Sign up. Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology.

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