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Home All issues Volume 31 / No 4 (2025) J Oral Med Oral Surg, 31 4 (2025) 36 Full HTML
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J Oral Med Oral Surg
Volume 31, Number 4, 2025
Article Number 36
Number of page(s) 7
DOI https://doi.org/10.1051/mbcb/2025039
Published online 09 December 2025

© The authors, 2025

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Introduction

The human immunodeficiency virus (HIV) disease is a true global pandemic. In 2023, an estimated 39 million people were living with HIV and 630,000 had died from opportunistic diseases [1].

The University Hospital of Clermont-Ferrand, France, has been caring for patients living with HIV (PLHIV) since the start of the epidemic in 1983. It is the regional reference center and hosts COREVIH Auvergne Loire, the regional committee for the fight against HIV and sexually transmitted infections. The active queue of PLHIV is approximately 2,000 patients, including patients referred from centers in the Allier, Cantal, Haute-Loire, Loire and Puy-de-Dôme departments [2].

The infectious diseases department and the odontology department of the Clermont-Ferrand University Hospital have been collaborating for decades in the care of PLHIV. These patients require even more diligent monitoring and support for oral care than uninfected patients as they are more likely to develop either tumors or opportunistic lesions due to their co-infection, comorbidity, and lifestyle, and to the weakening of their immune system [3]. Certain lesions of the oral mucosa are linked to a worsening of HIV or the appearance of a comorbidity and can be indicative of an HIV-related infection. Unfortunately, there is still discrimination in the management of PLHIV by dental surgeons [4], albeit to a lesser degree than before [5]. It is thus important that dental surgeons have a better understanding of HIV and concurrent associated oral lesions as they can play a key role in detection and thereby enable patients to be referred to a healthcare professional for early and appropriate care. Greater awareness of the problems encountered by PLHIV is now therefore a public health issue.

The present study was carried out to describe the prevalence of lesions of the oral mucosa at the beginning of the 2000s and in 2022 in PLHIV followed in the infectious diseases department of Clermont-Ferrand University Hospital.

Materials and methods

Regulatory aspect

Data collection from 1999 to 2002 (single-center, retrospective, cross-sectional study) was approved by the local Ethics Committee under number 2024-CF-267 (IRB00013412, “CHU de Clermont Ferrand IRB #1”).

The data from October 2021 to April 2022 (single-center, prospective, cross-sectional study) were collected in accordance with the reference methodology MR003. The protocol and the information letter were read and approved by the CPP (Committee for the Protection of Persons) Sud-Ouest et Outre-Mer on 04/10/2021 (RCB ID no.: 2021-A01831-40 – CPP 1-21-087/21.02369. 000034). The Clermont-Ferrand University Hospital, promoter of the study, notified the National Agency for the Safety of Medicines and Health Products of the approval of the CPP. The study was registered under clinical trial number NCT05123547.

Patients

We enrolled adult patients infected with HIV who had been followed in the infectious diseases department of Clermont-Ferrand University Hospital from 1999 to 2002 and from October 2021 to April 2022.

Data of PLHIV with oral lesions from the group followed between 1999 and 2002 were collected retrospectively by consulting medical files. Oral lesions present at the time of their (quarterly) consultation were noted systematically by the specialist doctor (CJ) and confirmed by the examination of a single oral surgeon (LD). The lesions were taken into account in the grading of the stage of the disease (grades B and C of the classification of the Center for Disease Control and Prevention) [6].

The 2022 data were obtained by an intraoral clinical examination and a questionnaire completed orally during the biannual consultation. All patients were invited orally by their specialist doctor, who was the same as in 2002 (CJ), to participate in the study and then in writing to ensure that their informed consent was given freely. Patients who accepted were redirected to another consultation room where they were all received by the same dental surgeon supervised by the oral surgeon present in 2002 (LD). Some PLHIV included were non-French nationals who spoke no or very little French and formed a subgroup that only underwent the clinical examination in order to meet the primary objective. They therefore did not complete the questionnaire, which was recorded as missing data.

Data

Data from each patient were collected on an anonymized computerized questionnaire. The data of the 2000s group were extracted with Epi InfoTM software (version 6), which processed the epidemiological data in the form of a questionnaire. This sheet served as a support for recording the variables studied.

In 2022, the questionnaires were immediately anonymized and numbered in order of arrival of patients. The data were then transferred to REDCap software (Research Electronic Data CAPture, Copyright 2006–2013 Vanderbilt University) with the corresponding number. The variables necessary for the study were retrieved from the observation notebook containing the medical file of each patient.

Demographic and medical data

The socio-demographic variables of age, sex and professional situation were collected for each patient. The following medical data were also collected: heterosexual/homosexual mode of contamination, under antiretroviral (ARV) treatment, lifestyle habits (tobacco, alcohol, drug consumption), latest viral load, and most recent LTCD4 counts.

Oral mucosal pathologies

The same oral surgeon (LD) performed the biopsies and made the various diagnoses of oral mucosal lesions in 2002 and 2022.

In the 2000s group, the diagnosis of oral lesions recorded in the patient files was made by the specialist doctor (CJ) and then confirmed by the oral surgeon (LD) from the Odontology Department of Clermont-Ferrand University Hospital at each clinical examination. In 2022, a clinical examination was carried out by a dental surgeon to observe all oral mucosal lesions. If there was a lesion in the oral mucosa, a photograph was taken, revealing only the lower half of the face. In order to preserve anonymity, the latter was identified by a patient code. The photograph made it possible to subsequently confirm the diagnosis by the oral surgeon from the Odontology Department.

The study was based on a classification by score already used elsewhere [5–7]. The scores comprised: 1 = lesions not related to HIV for which no current evidence shows a link with HIV; 2= indicative lesions/particular progression due to HIV listed in the oral manifestations related to HIV by OHARA (the Oral HIV/AIDS Research Alliance) but not classified as CDC stages B and C [7], and lesions that can emerge during long-term immunosuppression in HIV infection and appear suspicious when they are present chronically but which can also be explained by the presence of associated comorbidities, lifestyle and environment; 3= HIV-related lesions, which are classified as stages B and C in the CDC classification and listed in the oral manifestations related to HIV by OHARA [6,7].

Between 2002 and 2022, if a lesion appeared suspicious, a consultation was offered to the patient to carry out a more thorough clinical examination and a biopsy with a view to establishing adequate treatment and/or support.

Lesions classified as CDC scores 2 and 3 were all identified on histological criteria upstream, except for candidiasis, herpes labialis, and oral aphtosis. Score 1 lesions were only biopsied if the clinical examination did not allow their diagnosis with certainty.

Statistical analysis

Statistical analyses were performed with Stata software (version 15; StataCorp, College Station, TX, USA). All tests were two-sided with an alpha level set at 5%. Categorical data were expressed as frequencies and associated percentages, and age as mean. The two sets of samples (2000s and 2022) were compared with chi-squared test or Fisher's exact test for categorical data.

Results

Demographic and medical data (Tab. I)

In total, 62 PLHIV were included in the 2000s sample, and 112 PLHIV in the 2022 group, with an average age of 38.1 yr and 54.0 yr, respectively (p=NA). The patients were predominantly male: n=49/62(79.0%) and n=80/112(71.4%), respectively, for the two groups (p=0.27). In 2022, we observed a greater proportion of patients who were economically active than in 2002, 54.2%(n=58/107) vs 35.5%(n=22/62), respectively (p=0.02).

Between 2002 and 2022, there was a non-significant increase in heterosexual transmission (33.9% vs 42.7%), tobacco use (38.7% vs 50.5%) and drugs use (17.7% vs 20.6%), and a significant increase in alcohol consumption (6.5% vs 28.0% p=0.001). In 2022, all the PLHIV were receiving ARV treatment compared to 24.2% in 2002, (p<0.001), and more of them had a LTCD4 count >350/mm3(87.5% vs 8.1% in 2002, p<0.001) and an undetectable viral load (91.1% vs 4.9%, p<0.001).

Table I

Comparison of socio-demographic and medical characteristics of patients from the two periods (2000s and 2022).

Lesions of the oral mucosa (Fig. 1)

Clinical examinations identified 63 oral lesions in 62 PLHIV in the 2000s and 23 lesions in 22 PLHIV in 2022. In 2002, the lesions were distributed as follows: 87.3% with score 3, of which n=46/55 were candidiasis and n=9/55 oral hairy leukoplakia; 11.1% with score 2, of which n =1/7 were xerostomia, n=2/7 oral ulcers and n=4/7 labial herpes; and 1.6% with score 1. In 2022, the lesions were distributed as follows: 17.4% with score 3, of which n=2/4 were candidiasis, n=1/4 oral hairy leukoplakia and n=1/4 Kaposi's disease; 21.7% with score 2, of which n=2/5 were non-homogeneous leukoplakia, n=1/5 squamous cell carcinoma, n=1/5 warty papilloma and n=1/5 oral aphtosis; and 60.9% with score 1. Between the 2000s and 2022 groups, there was a significant decrease in HIV-related (score 3) lesions (87.3% vs 17.4%, p<0.001). Over a period of 20 yr, we observed a reduction in oropharyngeal candidiasis (73.0% vs 8.7%, p<0.001) and an increase in lesions with malignant potential and malignant lesions (Kaposi's disease, non-homogeneous leukoplakia and squamous cell carcinoma) (0.0% vs 17.4%, p=0.004).

thumbnail Fig. 1

Lesions of the oral mucosa.

Discussion

The two patient samples are homogeneous overall

Although the proportion of men and women were similar in the two samples, we found a male predominance (>70%) which was higher than that of PLHIV at the national level (64.3%) [2]. There was no significant difference in the figures for heterosexual transmission, tobacco and drugs use between the two periods. In contrast, we noted an aging of the PLHIV in 2022 (54.0 yr), which was consistent with the national average (53.1 yr) [2], compared to 2002 (38.1 yr). This aging of the population can be explained by the increased life expectancy of PLHIV, close to that of the general population, after the advent of ARV treatments [8]. The professional status of patients from the 2022 sample was less precarious since a significantly greater number of them were in active employment. However, they had higher alcohol consumption.

Disease control is different

One major change was in the uptake of ARV treatment: in 2022, all PLHIV were being treated as against less than a quarter in 2002(p<0.001). The current national average of PLHIV under treatment is 96.1%. In addition, immune status has been significantly restored (p<0.001). In 2022, the proportion of patients with a LTCD4 count >350/mm3 was 87.5% compared to 8.1% in 2002. Likewise for the viral load, since 86.9% of patients had an uncontrolled viral load (> 1000 copies per mL) in 2002 while in 2022 91.1% of patients (compared to 93% in France overall) had an undetectable viral load.

Thus, our patient sample of 2022, unlike that of the 2000s, did not fundamentally differ from the overall population of PLHIV in France [2] in terms of immune status.

The incidence of HIV-related oral lesions decreased in 2022 but their prognosis was more severe

Owing to the effectiveness of ARV treatments, the number of score 3 oral lesions has declined significantly over the last two decades, from 87.3% to 17.4% [9]. Thus, candidiasis, which accounted for 73.0% of oral lesions in 2002 was involved in only 8.7% in 2022. The 2002 results correspond to those of other studies from the same period in which up to about 80% of lesions were due to candidiasis [10], probably owing to the low number of PLHIV receiving ARV treatment at that time. In contrast, there was a sharp decrease in oropharyngeal candidiasis in 2022, which correlated with the rate of esophageal candidiasis (about 9%) already found in 2012 [11]. The most common fungal infection today is pneumocystosis whereas candidiasis is only in the 5th position of fungal infections after being among the most common lesions found previously [12]. It is therefore the incidence of all opportunistic diseases that has decreased over the years, as shown in a graph published by the French High Authority for Health (HAS), concerning the period from 2008 to 2021, of the 10 most frequent pathologies classified as being in the AIDS stage [13].

It is important that professionals with specialized knowledge of the oral cavity, dental surgeons in particular, get to examine these patients for lesions suggestive of HIV infection or treatment failure since the appearance of oral or even cutaneous-mucous lesions can indicate an impairment of the immune system typical of undiagnosed or untreated PLHIV [14,15]. Even if the lesions are few in number, they often have a poor prognosis, and can lead to conditions at risk of malignant transformation such as non-homogeneous leukoplakia or to malignant conditions such as Kaposi's sarcoma and squamous cell carcinoma.

In 2022 we recorded an increase in Kaposi's sarcoma whereas the HAS and other studies rather showed a decrease [13,16], probably because only oral manifestations of Kaposi's sarcoma were taken into account in our study. In 2002, no intraoral Kaposi's sarcoma was found, but the lesion was observed in four patients at the cutaneous level. This pathology cannot be entirely eradicated by viral load control and effective ARV treatment [17]. In contrast, unlike in other studies, we found no pigmented lesions due to ARV treatment [9].

Candidal lesions have thus markedly decreased but lesions requiring appropriate and complex management, such as squamous cell carcinomas of the head and neck, are more common among PLHIV than in the general population not infected with HIV [18].

The problem of the occurrence of lesions is addressed in the recommendations of the WHO and the World Workshop on Oral Health and Disease in AIDS on treatment/prevention policies for oral lesions that strengthen the promotion of oral health care among PLHIV [19].

The immune system seems to have been restored but not in its entirety

The number of oral lesions in 2022 was 23, a low percentage related to HIV (score 3), attributable to the good compliance of the PLHIV recruited during their medical follow-up and treatment. The decrease in the number of HIV-related oral lesions is therefore not unconnected with the advent of ARV therapies from 1996 onward and immune restoration. A reduction in oral manifestations related to HIV infection, particularly candidal lesions [20], had been observed since the appearance of ARVs before the 2000s [21]. In a study by Arriba et al. of 99 subjects, oral candidiasis decreased from 31% to 1% [20]. Current treatments are more effective, with fewer undesirable effects and hence better tolerance and more simplified administration which, in turn, improve treatment compliance [22]. In addition, they are prescribed for all HIV-infected persons without any criteria of immunosuppression, and as early as possible, thereby resulting in a drastic reduction in benign oral manifestations. These ARV therapies therefore allow HIV-positive patients to remain asymptomatic [23,24].

In contrast, the indicator lesions due to HIV (score 2) with a more severe prognosis have increased. Tobacco-related oral lesions are very common in PLHIV, particularly leukoplakia and oral cancer, and have a synergistic effect if there is also excessive alcohol consumption. Their incidence significantly increased over the 20 yr between the two study samples. Concomitantly, there was an aging of the population and an increase in alcohol consumption. The increase in the risk of cancer in this population is related to the increasingly advanced age of HIV patients, immunovirological control (viral replication, number and nadir of CD4), exposure to oncogenic viruses (HPV, HBV [hepatitis B virus], HCV [hepatitis C virus], EBV, HHV-8), and/or the consumption of toxic substances (such as alcohol, tobacco, or cannabis or other drugs) [17].

These findings could explain why in our study two non-homogeneous leukoplakias and one squamous cell carcinoma were observed in 2022 while no lesions of this type were detected in the 2000s. French and international epidemiological studies confirm an increase in the incidence of cancers among people living with HIV since 1990, including head and neck cancers, although the latter occur less frequently than the others [3,25].

PLHIV, despite restored immune status, remain more susceptible to tumor pathologies for which the tumor control mechanism has not yet been fully established. The incidence of oral and anogenital HPV lesions has increased under highly active antiretroviral therapy (HAART). Cell-mediated immunity is considered a key factor in wart regression, which is observed at the initiation of HAART treatment. In other cases, the warts persisted despite a significant increase in CD4 counts [26]. Comparison with a general population of the same age shows that HIV infection is associated with a greater number of age-related comorbidities such as cardiovascular, metabolic, pulmonary, renal, bone or tumor diseases [27]. Indeed, there are risk factors that are still not under control for which there is an urgent need to establish strategies, notably smoking and alcohol cessation, backed up by encouragement of universal vaccination against HPV in order to move toward a reduction in the prevalence of tumor lesions [28].

Limitations of the study

We are aware that our study may contain biases. One limitation is the partly retrospective nature of our work, in which we used a different method for obtaining data between the two periods. The main medical stakeholders were nevertheless the same (CJ for the infectious diseases content and LD for the odontology content), guaranteeing a certain homogeneity in the results obtained. It would have been interesting to compare certain data, in particular the level of precariousness, education or oral and dental follow-up but, unfortunately, they were not always available in the medical file.

Conclusion

Oral lesions among PLHIV are today less frequent. There has been a very clear overall improvement in the monitoring and treatment of these patients, who have a sufficiently high LTCD4 count to protect them from immunosuppression. They are no longer subject to opportunistic infections and are therefore less likely to have damage to the oral mucosa. The clinical feeling we had, that is to say a drastic modification of the oral lesions encountered, in particular the almost total disappearance of oral candidiasis (mostly found in the early 2000s), is confirmed by our results. However, certain lesions of the oral mucosa remain a diagnostic marker of HIV infection in patients unaware of their seropositivity or a diagnosis of severe comorbidity in PLHIV. This allows the dentist to play a key role in the early discovery of HIV infection or in early diagnosis of severe comorbidity and to offer the patient appropriate and early care, particularly when there is continuous communication between the infectious disease specialist and the dental surgeon. In the future, the challenge will be to control the risk factors of premature aging of people living with HIV while maintaining the good efficacy of ARV treatments, which have reduced the incidence of opportunistic diseases.

Funding

This article did not receive any particular funding.

Conflicts of interest

Nicolas Maubert declares that he has no conflict of interest.

Victoire Pinet declares that she has no conflict of interest.

Céline Lambert declares that she has no conflict of interest.

Émilie Goncalves declares that she has no conflict of interest.

Christine Jacomet declares that she has no conflict of interest.

Laurent Devoize declares that he has no conflict of interest.

Data availability statement

Data associated with this article cannot be disclosed due to ethical reason.

Author contribution statement

Nicolas Maubert contributed to investigation and wrote the main manuscript text with Laurent Devoize.

Victoire Pinet contributed to investigation.

Céline Lambert contributed to methodology and statistical analysis.

Emilie Goncalves contributed to Investigation.

Christine Jacomet and Laurent Devoize contributed to conceptualization, methodology, project administration and supervision.

All authors gave their final approval and agree to be accountable for all aspects of the work.

Ethics approval

All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

The data collection from 1999 to 2002 (single-center, retrospective, cross sectional study) was approved by local Ethics Committee under number 2024-CF-267 (IRB00013412, “CHU de Clermont Ferrand IRB #1”).

The data collected from October 2021 to April 2022 (single-center, prospective, cross-sectional study) are in accordance with the reference methodology MR003. Its protocol and the information letter were reviewed and approved by the CPP Sud-Ouest et Outre-Mer on 04/10/2021 (RCB ID no.: 2021-A01831-40 – CPP 1-21-087/21.02369. 000034) and the sponsor, Clermont-Ferrand University Hospital, notified the National Agency for the Safety of Medicines and Health Products. In addition, the study was entered in the protocol register (clinical trials No. NCT05123547).

Informed consent

All patients included in this study give their informed consent.

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Cite this article as: Maubert N, Pinet V, Lambert C, Goncalves É, Jacomet C, Devoize L. 2025. Comparison of the prevalence of oral lesions in patients living with HIV between 2002 and 2022: a single-center retrospective cross-sectional study. J Oral Med Oral Surg. 31: 36. https://doi.org/10.1051/mbcb/2025039

All Tables

Table I

Comparison of socio-demographic and medical characteristics of patients from the two periods (2000s and 2022).

In the text

All Figures

thumbnail Fig. 1

Lesions of the oral mucosa.
In the text

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