Factors Affecting Linear Gingival Erythema in People Living with HIVABSTRACT
Objective: To investigate factors influencing the occurrence of linear gingival erythema (LGE) in people living with HIV (PLHIV).
Material and Methods: A cross-sectional study was conducted at the Dental Hospital of Sultan Agung, Central Java, Indonesia. PLHIV who provided informed consent underwent oral clinical examination and history taking. Inclusion criteria included the presence of well-demarcated, band-like erythema along the gingival margin. Blood samples were collected to assess CD4 cell counts, while mucosal swabs were cultured on Sabouraud Dextrose agar to identify Candida spp. Multivariate analysis was performed using logistic regression with a 95% confidence interval.
Results: A total of 91 participants were examined, and LGE was identified in 35.2% of cases. Mycological analysis revealed that 33% tested positive for Candida spp. Multivariate analysis showed prevalence ratios for gender (PR = 1.44, p=0.423), smoking (PR = 0.432, p=0.314), alcohol (PR = 0.000, p=1.000), ARV duration (PR = 0.962, p=0.49), CD4 count (PR = 0.999, p=0.587), CFU Candida spp. (PR = 1.000, p=0.528), Candida spp. presence (PR = 0.638, p=0.182), and fungal burden (PR = 0.713, p=0.232).
Conclusion: The presence of linear gingival erythema in people living with HIV was not significantly associated with gender, lifestyle factors, antiretroviral therapy duration, CD4 count, or Candida spp. colonization.
Keywords:
Candida; HIV Infections; Acquired Immunodeficiency Syndrome; Gingivitis.
Introduction
The prevalence of linear gingival erythema (LGE) is significantly high among people living with HIV (PLHIV). Previous studies shows that between 50% to 80% of PLHIV have some form of periodontal manifestations, with LGE being one of the most commonly identified lesions [1,2]. LGE associated with Human Immunodeficiency Virus/Acquired immunodeficiency syndrome (HIV/AIDS) subjects. Since HIV/AIDS may be contracted by young adult people, the age distribution of LGE cases tends to be younger. Especially for those in their third and fourth decades, LGE may be related to various risk factors, such as sexual activity, that may increase the spread of HIV infection in the risk populations. The spreading HIV infection may cause immunodeficiency, and this condition will result in the oral manifestations that are probably found in HIV patients. The immunological response of those HIV patients may be the main factors that contribute to the oral lesions in PLHIV [3].
Linear Gingival Erythema (LGE) previously known as HIV-Gingivitis [4,5] is an oral manifestation of HIV infection [6]. LGE may strongly associate with immunodeficiency status in people living with HIV/AIDS. The clinical features of LGE, such as a red band at the gingival margin, no ulceration, and no pocketing or attachment loss, may mimic plaque-induced gingivitis. Moreover, the lesion does not disappear after periodontal treatment. Studies have shown that Candida spp. may cause erythema [4-6]. However, evidence that Candida spp. contribute to the aetiology of LGE is still unclear. Many studies have reported that the involvement of Candida spp., such as Candida albicans is the most frequently found species [7-11]. Involvement of Candida spp. in LGE related to Candida spp. may produce and secrete serine proteases that may be essential virulence factors in the initial events of colonization in biofilm formation [12].
The LGE in PLHIV may be associated with an immunosuppressive condition in HIV, which leads to changes in the oral microbiome and immune response, and contributes to LGE development [11,13]. Correlation between LGE and CD4+ T lymphocyte counts suggests that reduced immune function may worsen the severity of this condition [14,15]. Understanding these mechanisms could provide insights into managing LGE and the broader implications for periodontal disease in PLHIV.
The ARV may also be a risk factor for LGE, although antiretroviral therapy (ARV) has shown to enhance overall health outcomes for HIV-positive individuals [16,17]. Previous studies suggest that while ARV may reduce the frequency of opportunistic infections, it doesn't completely eradicate the risk of periodontal diseases, including LGE [18]. Hence, the effects of ARV on LGE remain unknown.
With the various conditions in the oral cavity of PLHIV, LGE found in individuals with HIV may be influenced by many risk factors. It is important to know which risk factors may contribute to LEG in PLHIV to have a better understanding of LGE and enhance the management of oral health in HIV-positive patients. Based on this reason, this study was conducted to investigate factors affecting Linear Gingival Erythema in people living with HIV.
Material and Methods
Study Design and Ethical Clearance
This cross-sectional study involves PLHIV who participate in an examination at the Sultan Agung Dental Hospital in Central Java Province, Indonesia. This research was approved by the Research Ethics Committee of Medical and Health Universitas Gadjah Mada - Dr. Sardjito General Hospital with referral number KE/FK/0723/202, and by the ethics committee of Sultan Agung Dental Hospital with referral number 810/F/RSIGMSA/VI/2022. All participants were informed about the study objectives, risks and benefits and signed an Informed Consent Form.
Participants and Data Collection
PLHIV were recruited during medical appointments, between August 2022 and August 2023. The inclusion criteria were PLHIV with the presence of erythematous on the gingival margin. PLHIV aged under 18 years were excluded.
All data regarding age, gender, antiretroviral medication, and social or personal history were obtained using a questionnaire. The clinical examination of the oral cavity of PLHIV was conducted by an oral medicine specialist with LEG, determined by the presence of well-demarcated erythema (band-like) on the gingival margin. To clinically validate the LGE, the oral medicine specialist also examined a photo of the suspected LGE lesion. All subjects also undergo a blood examination, which is then analyzed by flow cytometry for CD4 T cell count.
Yeast Isolation and Identification
Mucosal swabs at the gingival margin were performed from all subjects who had a suspected LGE lesion where there was clearly demarcated erythema (band-like). Mucosal swabs collected were seeded onto Sabouraud Dextrose agar, as described by Taverne-Ghadwal et al. [19]. A clinical microbiologist identifies Candida spp. and counts CFUs.
Data Analysis
All data were presented descriptively. A logistic regression model was then used to investigate factors that may affect linear gingival erythema. IBM SPSS software, version 25 (IBM Corp., Armonk, NY, USA) was used for the analyses.
Results
There were 91 PLHIV who presented with well-demarcated erythema (band-like) on the gingival margin; of these, 59 were men (64.8%) and the heterosexual participants represented 63.7%. A total of 87.9% of participants reported no smoking habits and 98.9% abstaining from alcohol. CD4 cell count ranged 18 to 1404 cells/mm3 (mean count 418.7581 cells/mm3) (Table 1).
The majority of individuals have been on ARV treatment for a considerable period, with a mean duration of ARV treatment of 4.7 years. However, others have been on ARVs for 20 years. The most common ARV regimen was Tenofovir/Lamivudine/Dolutegravir (58.2%), followed by Tenofovir/Lamivudine/Efavirenz (25.3%) (Table 1).
Mucosal swabs were performed at the gingival margin where there was clearly demarcated erythema (band-like), without fungal growth (54.9%). Candida albicans (33%) was the most common species isolated, followed by Candida non-albicans (12.1%). Furthermore, 22% of patients have a high fungal burden of Candida spp. (Table 2).
Linear Gingival Erythema was observed in 35.2% (n=32) of participants. The number of PLHIV with LGE was higher in males than in females. The prevalence ratio (PR) for LGE was 1.44 in males compared to females, but was not statistically significant (p > 0.05). Prevalence ratio of 1.27 for MSM compared to heterosexual individuals suggests a possible increased risk of LGE among MSM, but this difference was also not statistically significant (p > 0.05) (Table 3).
The prevalence ratio for smoking was 0.432 (95% CI = 0.085 - 2.210), suggesting a potential lower risk of smoking in the LGE group. Only 2 out of 32 individuals in the LGE group were smokers, suggesting a low smoking prevalence within this population. The PR for alcohol consumption was 0.000, indicating no statistically significant association. All 32 individuals in the LGE group reported no alcohol consumption (Table 3).
The PR of 0.962 during antiretroviral therapy suggests that the duration of ART was not significantly associated with LGE. This means that individuals on ART for longer periods did not have a significantly higher or lower risk of developing LGE than those on ART for shorter durations. The analysis did not show any significant differences in LGE prevalence among various ARV regimens. This suggests that the specific type of antiretroviral medication used was not a significant factor in the development of LGE (Table 3).
CD4 Counts (cell/mm3) showed a PR = 0.999 (95% CI = 0.997 to 1.001). There was no significant association between CD4 cells count and LGE (p > 0.05); CD4 cells did not significantly influence the presence or absence of LGE. The presence of any species of Candida, a type of fungus commonly found in the mouth, was not significantly associated with LGE. The amount of fungal growth was also not significantly associated with LGE presence (Table 3).
The number Candida spp. revealed no significant effect. The association between Candida spp. and the outcome was not statistically significant. Among the subcategories, No Growth was observed in 20 of 50 cases, Candida albicans in 10 of 30 cases, and Candida non-albicans in 2 of 11 cases. Additionally, the Fungal Burden data show a PR = 0.713 (95% CI = 0.410 - 1.242), which is not statistically significant. In this group, 20 of 50 cases had no fungal growth, 7 of 21 cases had low fungal burden (1 - 15 CFU), and 5 of 20 cases had a high fungal burden (more than 15 CFU) (Table 3).
Discussion
This study showed that among 91 people living with HIV (PLHIV) participants, predominantly men (63%) identified heterosexual as their primary risk factor for HIV transmission. This is similar to the fact that heterosexual contact is the main risk factor in HIV transmission in other studies [8,20]. The second risk factor was PLHIV who have men who have sex with men (MSM) sexual activity and other risk groups, including bisexual individuals. Furthermore, this study found that IVDU, and transgender individuals, though in smaller numbers, highlight the complex and diverse nature of HIV transmission. This result may explain the risk factors that may also contribute to linear gingival erythema (LGE).
According to CD4 cells count number examination, the PLHIV in this study have a relatively healthy immune system, with CD4 cells count below the normal range of 500 to 1500 cells/mm3. However, some subjects have very low and very high CD4 counts, indicating wide variability in immune condition among participants. The level of serum CD4 cell count may reflect the immune status in HIV infection among PLHIV.
The prevalence of LGE in this study was 35.2%, with a higher prevalence in males than in females (PR = 1.44). However, there was no statistically significant difference between men and women (p > 0.05). The ratio for MSM compared to heterosexual individuals was 1:27. The result may suggest the increased risk among MSM, yet this finding also lacked statistical significance (p > 0.05). These results indicated that, while there may be trends suggesting higher prevalence rates in certain demographics, the lack of statistical significance calls for cautious interpretation and further investigation into the underlying factors contributing to these observations [21,22].
The study also found a prevalence ratio of 0.432 for smoking, which indicated a potential lower risk in the LGE group. However, the smoking did not show a significant result (p > 0.05). No association was observed with alcohol consumption. The low prevalence of smoking and alcohol consumption within this population may reflect the overall health-conscious behaviour of the participants, which could mitigate the risk of developing LGE [18,23]. Low smoking and alcohol consumption rates may indicate a healthy lifestyle among participants, which could contribute to better overall oral health. Previous studies shown that lifestyle factors, such as smoking and alcohol consumption, can worsen the health complications linked to HIV [24,25]. However, the lack of significant associations between smoking, alcohol consumption, and LGE suggested there may be other underlying factors that confound the result, which may decrease the progression of LGE.
The primary antiretroviral therapy (ART) regimen used was a combination of Tenofovir/Lamivudine/Dolutegravir (58.2%) according to current treatment guidelines due to its effectiveness and tolerability [26,27]. Interestingly, the study found no association between the duration of ART and LGE, suggesting that prolonged ART may not be directly associated with LGE prevalence. This crucial finding suggested that other factors, such as individual immune responses and co-infections, might play a more significant role in the development of LGE [28,29].
A decline in CD4 cells in people living with HIV (PLHIV) results in a decreased ability of the immune system, such as polymorphic nuclear neutrophils, to control the accumulation of Candida spp. in the subgingival area of PLHIV. The reduction in CD4 cells may predispose to an increase of the colonies of Candida spp. [30-32]. The accumulation of Candida hyphae triggers the excessive secretion of inflammatory mediators (such as metalloproteinases, IL-6, IL-8, and IL-1β) in the periodontal pockets of PLHIV. This condition allows for the development of LGE lesions [33]. On the contrary, the findings of this present study showed different results.
The wide range of CD4 cells counts showed the diverse immune status within the group. A mean count of 418.76 cells/mm3 suggests relatively healthy immune systems. The presence of both very low and very high counts indicated significant variability. The analysis of CD4 cells counts revealed no significant association with LGE (p > 0.05). This suggested that the CD4 cell count, a key indicator of immune function in HIV infection, did not differ significantly between those with and without LGE. This finding did not corroborate the evidence that lower CD4 cells counts would correlate with higher prevalence of oral manifestations of HIV/AIDS, which indicates other factors may be a confounder for LGE [34,35].
The study subjects who received ARV treatment, approximately 97.8%, consisted of Duviral, Lamivudin, Neviral Duviral, the combination of Tenofovir-Lamivudine-Dolutegravir (TLD), and the combination of Tenofovir-Lamivudine-Efavirenz (TLE). These ARV drugs contain NRTI (nucleoside reverse transcriptase inhibitors) [26]. PLHIV receiving NRTI ARV treatment and having CD4 > 300 cells/mm3 prevent the disruption of cytokines production Th1/Th2/Th17 and Human beta defensin 2, and reduce the risk of oral candidiasis [32].
The high rate of Candida albicans isolation (33%) from LGE lesions suggests its potential role in LGE development. The high Candida albicans prevalence observed in 22% of participants may also be a risk factor for oral candidiasis in PLHIV [36,37]. These findings also supported the evidence that Candida spp. involvement is an opportunistic infection in PLHIV.
This study found no significant association between Candida species and LGE, leading to uncertainty about the role of fungal infections in causing LGE. Previous studies have indicated that while Candida spp. can contribute to oral lesions in immunocompromised individuals. The role of Candida species in LGE development may not be significant [38,39]. The persistence of erythema on the gingiva, even with low fungal growth, indicated that other microbial or host immune factors could be contributing to the lesions' development and persistence. This study highlighted the prevalence and associated risk factors of linear gingival erythema in PLHIV, showing the complexity of its causes.
However, this study had a limitation: participants were from a single province in Indonesia, which may limit the generalizability of the findings. Consequently, the results might not accurately reflect the national incidence of LGE or the broader risk profile among PLHIV across Indonesia. Further studies with larger sample sizes across other areas and detailed longitudinal studies are essential to understand the mechanisms underlying LGE and to develop targeted treatments. Future studies should aim to explore longitudinal data to better understand the dynamics of oral health in relation to HIV progression and treatment.
Conclusion
No risk factors for the linear gingival erythema in people living with HIV were found, which may explain the mechanisms contributing to this condition in these individuals.
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Financial Support
The authors sincerely thank Universitas Gadjah Mada for financially supporting this research via the Rekognisi Tugas Akhir (RTA) Program of Batch 1 (No: 3550/UN1.P.III/Dit-Lit/PT.01.05/2022).
Acknowledgments
The authors extend their deepest gratitude to the participants who took part in the study and the three Oral Medicine specialists who validated all the LGE cases identified.
Data Availability
The data used to support the findings of this study can be made available upon request to the corresponding author.
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Edited by
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Academic Editor:
Alessandro Leite Cavalcanti
