Characteristics of oral mucosal lesions and their association with socioeconomic status and systemic health in a remote rural area in China: a cross-sectional study of 146 cases

Epidemiological data of oral mucosal lesions (OMLs) are required to develop practical oral care policies. However, limited data are available for rural areas in China. We aimed to estimate the spectrum and prevalence of OMLs and to identify their associated socioeconomic status (SES) and systemic health in a remote rural area in Yunnan, China. We screened patients for OMLs in an oral medicine clinic in rural Yuannan, China, from August 2020 to February 2021. OMLs were documented. SES, including the highest education level achieved and the previous month’s household income, as well as the patient’s systemic health, including a history of smoking, alcohol use, and chronic disease, were obtained from the Medical History/Health Questionnaire Form and patient medical records.


Conclusions
In rural Yunnan in China, the most frequent OML was aphthous ulcer, which was followed by BMS, viral ulcer, and OLP. Chronic diseases were associated with BMS. Age was an independent protective factor for oral viral ulcers. A high-income level was associated with the presence of OLP. Oral care policies should be prioritized among patients with aphthous ulcer. Preventive strategy of BMS should be targeted to people with chronic disease for health equalities.
Background Page 3/18 Oral mucosal lesions (OMLs) include various disorders involving the oral mucosa, affecting 4.9-64.7% of people in the general population worldwide [1]. Some lesions can impair chewing, swallowing, and speaking functions [2], while others may in uence systemic health [3] or progress to oral cancer [4]. The Chinese government released the Healthy China 2030 blueprint to guide the healthcare promotion [5]. Oral health is an important part of this blueprint. To promote oral health, manage oral diseases, and develop an oral care strategy, it is urgent for governments to understand local epidemiological characteristics of OMLs.
In the rural areas, patients with OMLs often suffer more due to their di culty with accessing appropriate oral healthcare in a timely manner. The epidemiology of OMLs is also not well characterized in remote rural areas due to a lack of local oral specialists. Recently, the Shanghai and Yunnan governments organized a program for oral specialists to temporarily work in these rural areas and perform free oral examinations in the local population. This provides an opportunity to understand the characteristics of OMLs in local rural areas.
In this study, we aimed to determine the spectrum and frequency of OMLs along with their possible associations with socioeconomic status (SES) and systemic health in a remote rural area in Yunnan, China. Our study results provide preliminary epidemiological data for policy making to improve oral hygiene in this local rural area in China.

Study setting and participants
The present study was performed in a rural Oral Medicine Clinic ran by the Department of Stomatology, the People's Hospital of Xiangyun a liated with Dali University, China. This clinic included an oral medicine specialist who stationed, practiced, and trained two general dentists there between August 2020 and February 2021. With the support of the poverty-alleviation program collaborated by Shanghai and Yunnan, the specialist worked there and provided free oral examinations. The ethics committee of the People's Hospital of Xiangyun approved this study (no. 2020069). All patients and/or their guardians signed informed consent. We included all patients with OMLs and excluded all visitors without OMLs. alcohol use, and chronic disease. These variables were used as exposures to analyze whether they were associated with OML outcomes.
The diagnostic criteria for OMLs were based on the fourth edition of Oral and Maxillofacial Pathology authored by Neville B. et al. In the dental o ce, an oral examination was performed under a dental chair light with the patient sitting on the chair. The specialist inspected and palpated using tools including a mirror, explorer, cotton swab, and sterile gauze. The specialist adopted the following examination sequence: face, lip, buccal, tongue, mouth oor, hard palate, soft palate, gum, and alveolar ridge. When the diagnosis was uncertain, we marked "diagnostic uncertainty" in the medical records due to a lack of oral pathology or other laboratory services in the rural hospital.

Statistical analysis
Age is presented as a median with interquartile range (IQR). Categorical variables are presented as numbers with percentages (%). Unadjusted or adjusted regression analyses were performed to analyze the risk factors (sex, age, education, the last-month household income, smoking, alcohol use, and chronic disease) associated with the presence of OMLs. Statistical analyses were conducted using SPSS software (version 26.0, IBM Corporation, Armonk, NY, USA). Statistical signi cance was set at P < .05.

Discussion
In this study, we found the most common OMLs were aphthous ulcer, BMS, and viral ulcer. The most common comorbidities were sleep apnea, hypertension, and bronchitis (including emphysema). Patients with chronic diseases had a higher prevalence of BMS compared without those without chronic diseases. A household income of less than 6,000 yuan was an independent risk factor for OLP. These major ndings can provide practical information for the government to optimize medical resources during the prevention and intervention of OMLs in remote rural areas where oral services are limited.
In terms of the relative frequency of OMLs, ndings vary in the literature due to different diagnostic criteria, participants, and study methods. Patients with or without pathogen cultures and histopathological examinations might have different diagnoses. The use of a community-based survey or a medical records review could also cause certain analysis biases, such as participants enrolled. Overall, aphthous ulcer, BMS, and OLP were the most frequent OMLs [6,7]. Oral submucous brosis was not found in our study, but its frequency is high in some regions of China, such as Hunan [8], probably due to the common habit of chewing betel nuts. The present study also showed that 24.0% our study population had sleep apnea, which was the most common comorbidity. This is consistent with the prevalence of sleep apnea in the general population [9]. Other common comorbidities were hypertension, bronchitis (including emphysema), re ux (including gastroesophageal re ux disease), and arthritis. The life and work routines might explain the frequency of comorbid diseases. People in our survey area had a high prevalence of sleep apnea and were more likely to have frequent smoking and/or drinking habits, which increased their risk for hypertension. A certain number of people in our survey area smoked and worked in the mining industry; thus, it is common for them to have lung diseases. Re ux mostly affected people who work in mountains for extended periods and skipped their meals. Prolonged standing or lengthy climbing up and down during work increases the risk of arthritis. This nding about comorbidities was also consistent to the spectrum of chronic disease in a study from China [10].
Aphthous ulcer is among the most common OMLs, with a prevalence of approximately 20% [11] and an incidence ranging from 5-50% [12]. Smoking is its protective factor [13,14]. Our study also supported such relationship between smoking and aphthous ulcer on unadjusted regression analysis. However, this association disappeared after adjusting for multiple confounders. The reason for this loss might be that the causes of aphthous ulcer were comprehensive and multifactorial, including a genetic background, stress, and nutritional de ciencies [15]. Viral ulcers in the mouth affected more than 85% of adults [16]. Additionally, 40% of patients with primary herpetic simplex virus (HSV) experienced recurrent HSV infection [17]. There was a signi cant age-related decrease in the frequency of viral ulcer after adjusting for sex, the highest education level achieved, the previous month's household income, smoking, alcohol use, and chronic diseases in our study. The reason for this might be because primary HSV infection was common in children aged six months to ve years and young adults aged 20 years [18]. Some associations were found between chronic disease and viral ulcer on unadjusted regression. The explanation for this association could be that recurrent HSV infection happened from its latent forms in the trigeminal ganglions during a host's immunocompromised or immunosuppressed state [19,20]. However, no interaction was identi ed between chronic disease and viral ulcer in the context of sex, age, highest education level achieved, previous-month household income, smoking, or alcohol use. It is notable that oral viral ulcers can also happen in patients without chronic diseases. The causal relationship between oral viral ulcers and chronic disease requires further investigation.
The prevalence of BMS in the general population was estimated to be between 0.7% and 8% based on different diagnostic criteria [21,22]. In the current study, we found that chronic disease increased the risk of developing BMS after adjusting for sex, age, highest education level achieved, previous-month household income, smoking, and alcohol use. The reason for this could be that systemic factors, including anemia, diabetes, thyroid disease, hormonal de ciency, upper respiratory tract infection, gastroesophageal re ex disease, Parkinson's disease, and side effects of antihypertensive medications, were associated with BMS [23].
OLP is a chronic in ammatory condition, which is a common mucocutaneous disorder in the oral cavity.
The prevalence of OLP was estimated to be between 1% and 3% [24]. Systemic factors, such as hypertension, diabetes, viral infection, autoimmunity or immunode ciency, and cancer, were supposed to be its etiology [24]. Patients with OLP had signi cantly higher prevalence of stress, anxiety, and depression than the general population [25][26][27]. A chronic and long-lasting course of OLP could make patients stressed, anxious, and depressed. Meanwhile, stress, anxiety, and depression could lead to the development of OLP. Furthermore, there might be an association between depression and high income, although this suggestion contradicted other study results [28][29][30]. People with high incomes may perform high-pressure work in a competitive environment. Depressed individuals with high income levels may have an increased risk for developing OLP. However, this association should be treated with caution because chronic disease can reduce the associations of SES factors, such as income, with depression [28][29][30]. The underlying mechanism needs to be explored further.
Our study had some limitations. The small sample size could cause biases in our result analysis. Some patients might have oral lichenoid lesions that were di cult to distinguish from OLP without laboratory con rmation. Therefore, the frequency of OLP might be overestimated. All diagnoses were made by one single specialist. Thus, the reliability of the diagnoses might be weakened.

Conclusions
In conclusion, we demonstrated the frequency of different OMLs in rural Yunnan and found that aphthous ulcer was the most common OML, which was followed by BMS, viral ulcers, and OLP. Older age had a decreased risk for oral viral ulcers. Chronic diseases were associated with a signi cant increase in BMS, and a high-income level was associated with OLP. Priority of oral care policies should be given to patients with aphthous ulcer. Preventive interventions of BMS should be developed among people with chronic disease. We have con rmed that the study protocol was approved by the ethics committee of the People's Hospital of Xiangyun (no. 2020069) and informed consent was obtained from all patients and/or their guardians.

Abbreviations
We have also con rmed that all methods were carried out in accordance with the ethical standards in the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

Consent for publication
Not applicable. No personal information was provided in this paper.

Availability of data and materials
The data and materials collected in this research are not publicly available due to privacy and ethical restrictions. But they are available from the corresponding author upon reasonable request.

Competing interests
The authors reported no competing interests.

Funding
This study had no funding.

Authors contributions
H. Y., M. L., and G. T. formulated the conception and designed the study. H. Y., Q. Z., Q. S., and M. L. acquired, analyzed, and interpreted the data. G. T. and H. Y. drafted the manuscript. All authors have