Dentition, oral hygiene, and risk of oral cancer: a case-control study in Beijing, People's Republic of China

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1 Cancer Causes and Control 1, Dentition, oral hygiene, and risk of oral cancer: a case-control study in Beijing, People's Republic of China Tongzhang Zheng, Peter Boyle, Huanfang Hu, Jun Duan, Peijue Jiang, Daquan Ma, Liangpeng Shui, Shiru Niu, Crispian Scully, and Brian MacMahon (Received 24 July 1990; accepted in revised form 28 August 1990) A case-control study of oral cancer was conducted in Beijing, People's Republic of China. The study was hospitalbased and controls were hospital in-patients matched to the cases by age and gender. A total of 404 case/control pairs were interviewed. This paper provides data regarding oral conditions as risk factors for oral cancer, with every patient having an intact mouth examined (pre-operation among cases) using a standard examination completed by trained oral physicians. After adjustment for tobacco smoking and alcohol consumption, poor dentition--as reflected by missing teeth--emerged as a strong risk factor for oral cancer: the odds ratio (OR) for those who had lost teeth compared to those who had lost none was 5.3 for men and 7.3 for women and the trend was significant (P < 0.01) in both genders. Those who reported that they did not brush their teeth also had an elevated risk (OR = 6.9 for men, 2.5 for women). Compared to those who had no oral mucosal lesions on examination (OR ), persons with leukoplakia and lichen planus also showed an elevated risk of oral cancer among men and women. Denture wearing per se did not increase oral cancer risk (OR = 1.0 for men, 1.3 for women) although wearing metal dentures augmented risk (OR = 5.5 for men). These findings indicate that oral hygiene and several oral conditions are risk factors for oral cancer, independently of the known risks associated with smoking and drinking. Key words: Alcohol, case-control study, dentition, leukoplakia, lichen planus, oral cancer, oral hygiene. Introduction Even though oral hygiene, inadequate dentition reflected by loss of teeth, jagged teeth, septic and decayed teeth, and oral mucosa lesions such as leukoplakia have long been suspected to be risk factors for oral cancer, 1-10 the role of such variables has been overshadowed for a long time by the results of studies relating tobacco smoking, alcohol drinking and, in Eastern countries, betel chewing to oral cancer risk. 11'12 The independent and joint effects of these factors with tobacco smoking and alcohol drinking have not been studied extensively. Therefore, a hospital-based case-control study was conducted in Beijing to evaluate the possible role of oral hygiene and dental conditions, as well as tobacco smoking, alcohol drinking, diet, and nutrition in the genesis of oral cancer. Here we report the data relating to oral hygiene and dental conditions. From the Department ofepidemiology, National Institute ofenvironmental Health and Engineering, Chinese Academy of Preventive Medicine, Beijing, China (ZT; HH; NS); Unit of Analytical Epidemiology, International Agency for Research on Cancer, Lyon, France (PB; ZT); Belying Union Hospital (DJ); Cancer Institute, Chinese Academy of Medical Science (]P); Beijing Medical University Stomatological Hospital (MD); Bei]ing Municipal Stomatological Hospital (SL); University Department of Oral Medicine and Oral Surgery, Br~tol Dental Hospital and School, UK (CS); Department of Epidemio/ogy, Harvard School of Public Health (BM; ZT). Address correspondence to Dr Zheng at the Cancer Prevention Research Unit, Yale University, School of Medicine, 26 High Street, New Haven, CT 06510, USA. Dr Zheng was partly supported by a grant from the DuPont Company Rapid Communications of Oxford Ltd 235

2 T. Z/aeng et al. Materials and methods A description of the study design has been given previously. 13 Briefly, cases consisted of all the male and female incident oral-cancer patients admitted to any one of the seven hospitals that treat oral cancer in Beijing. A total of 404 patients with histologically confirmed oral cancer (ICD-9 TM codes 141 [cancer of the tongue] and [other parts of the mouth, excluding salivary gland; pharynx including nasopharynx]) were interviewed between 1 May 1989 and 24 December The cases ranged in age from 18 to 80 years at the time of diagnoses. One control was selected for each case matched on hospital, gender, and age within five years. Controls were randomly chosen from patients whose current hospitalizations were for minor conditions diagnosed within one year and believed not to be associated with the exposures of interest. The diagnoses in the controls included minor surgery (e.g. hemorrhoids, strangulated hernia, etc.), ophthalmic and ear conditions, low back pain, urinary tract infection, and some other conditions. There were no refusals to participate in either the cases or their 404 first-selected controls. A standard structured questionnaire was used to obtain information on prior use of tobacco and alcohol, and occupational and environmental exposures, as well as other relevant factors. Interviews were conducted in person by two trained, retired nurses who had no knowledge of the study hypotheses. At each participating hospital, there was one dentist who was responsible for the histologic confirmation of all the cases, oral examination for all the cases and controls of that hospital, and completion of a brief questionnaire, as an addendum to the main questionnaire, including detailed questions on dentition, oral hygiene, and the presence of oral mucosa lesions. Questions included: how often the patients visited a doctor because of toothache, oral ulceration, or for a routine dental check-up; the frequency of tooth brushing or denture cleaning; the number of years elapsed between loss of teeth and having dentures fitted, and the number of years of denture-wearing. Oral examination included: recording of the number of missing teeth, jagged teeth, filled teeth, decayed and septic teeth; the presence of gingivitis or periodontal disease and other oral mucosa lesions including leukoplakia, erythroplasia and lichen planus. All the interviews and oral examinations were conducted before surgery. When a questionnaire was completed and sent back to the research center by an interviewer, a quality controller (who was also a dentist) would check the accuracy of the coding and completeness of questionnaires. The correction of errors and collection of missing information were undertaken by going back to the hospital and re-interviewing the case or the control. As 236 with the interviewers, the doctors and quality controller were not informed about the particular hypotheses being evaluated. The exposure odds ratio (OR) was used to estimate the relative risk of oral cancer associated with each risk factor. The crude OR (ORc) and the corresponding confidence interval (CI) were calculated using the method of Mantel and Haensze115 for each level of the exposure of interest. In the text, numbers in parentheses following an OR are 95 percent CI of the OR. The adjusted OR (ORa) was obtained from conditional logistic regression analysis containing both the exposure variable and potential confounding factors. 16 The following potential confounding factors were included in all the models: (i) alcohol drinking (using total lifetime kgs of spirit-equivalent consumption in five categories for men and three categories for women); (ii) tobacco smoking (using pack-years of cigarette-equivalent smoking in five categories for men and three categories for women); (iii) years of education used as an indicator of socioeconomic status in four categories for all analyses. Gender and age were matched variables. When the condition of the dentures worn and the risk of oral cancer were assessed, the length of denture wearing in four categories was also included in the model. Formal statistical assessment of effect modification between dentition, tobacco smoking, and alcohol drinking was conducted by using conditional logistic regression analyses controlling for education, gender, and age. Tests for trend were performed by treating each variable in the model as a continuous variable and the ratio of the estimated coefficient to its standard error obtained from the model was used to make statistical inferfence based upon a two-sided alternative hypothesis at the five percent level of significance. Results The crude and adjusted ORs for denture wearing and the risk of oral cancer for men are given in Table 1. As shown in this table, no significant association was observed between oral cancer risk and the use of dentures, either partial or complete. No association with oral cancer risk was found either with years of denture wearing or years elapsed between teeth extraction and having a denture fitted. Regarding the type of material used in the manufacture of the denture, more cases than controls wore dentures made of metal (ORa of 5.5), but the number of subjects who had this type of denture was small and the excess not significant (CI ). Table 2 presents the data for females. The same trends that were seen among males are evident. No statistically significant association was found between wearing dentures and the risk of oral cancer.

3 Oral cancer in China Table 3 describes the association between the condition of the dentures and the risk of oral cancer. Even though having a denture did not show any association with oral cancer, the condition of the denture gave some indication of being a risk factor. For both men and women, more cases than controls needed to have a denture repaired or rebased, with an OR of approximately two for having a denture which needed Table 1. Dentures and the risk of oral cancer in males Risk factor Cases Controls ORe a ORa b 95% CI Having denture No i Referent Yes partial complete Interval c > Years d ,5-2.2 > Materials Vulcanite 0 0 Plastic Metal acrude OR. C of years between loss of teeth and fitting of denture. d of years denture worn. Table 2. Dentures and the risk of oral cancer in females Risk factor Cases Controls ORe a ORa b 95% CI Having denture No Referent Yes partial complete Interval c > Years d > ,4-2.6 Materials Vulcanite 1 0 ND - Plastic Metal 7 0 ND - acl!ade OR. C of years between loss of teeth and fitting of denture. d of years denture worn. ND, not determinable. 237

4 T. Ztseng et al. Table 3. Denture condition and risk of oral cancer Risk factor Cases Controls ORc a ORa b 95 % CI MEN Need repair No ,0 Referent Yes ,8-4.9 Need rebasing No ,0 1.0 Referent Yes WOMEN Need repair No Referent Yes ,7-9.1 Need rebasing No Referent Yes ~Crude OR. bor adjusted by conditionallogistic regression fortobacco smoking, alcohol drinking, education, number ofyears wearing denture, gender, and age. Table 4. Loss of teeth and the risk of oral cancer in males Risk factor Cases Controls ORc" ORa b 95% CI No lost teeth Referent Lost with Lost without of lost teeth , of lost teeth with , of lost teeth without ~Crude OR. bor adjusted by conditional logistic regression for tobacco smoking, alcohol drinking, years of education, gender, and age. 238

5 Oral cancer in China to be repaired and/or rebased after adjustment for years of denture wearing and other major confounding factors. However, although all four ORs were high, each CI included the value 1.0. Table 4 presents the data relating loss of teeth to risk of oral cancer for males. Having lost teeth, regardless of or not, was associated with increased risk for oral cancer, with an OR of 2.4 ( ) for the former and 3.7 ( ) for the latter. For the number of lost teeth, an increased risk with increasing number of lost teeth was noted, which is even more pronounced for having lost teeth without ; tests for trends are significant at P < Table 5 presents the same data for females; a similar trend but a much stronger effect of loss of teeth on the risk of oral cancer was noted. Oral hygiene, as reflected by whether teeth were brushed, is strongly associated with the risk of oral cancer (Table 6). An adjusted OR of 6.9 ( ) for men and 2.5 ( ) for women were found for those not brushing their teeth compared with those brushing their teeth once or more per day. The results in Table 7 suggest a strong association between oral leukoplakia, lichen planus, and risk of oral cancer. Among males, more than seven percent of the cases were found to have leukoplakia compared with less than 0.5 percent of the controls, and 10 percent of the cases were found to have lichen ptanus compared with less than one percent of the controls. For females, even though six percent of the cases were found to have oral leukoplakia and nine percent of the cases were found to have lichen planus, no controls were found to have either of the diseases. On the other hand, the great majority of cases of oral cancer occurred in the absence of any of these lesions. Table 8 presents the associations of oral cancer with inadequate dentition, tobacco smoking, and alcohol drinking considered singly or in combination. In these analyses, inadequate dentition was defined according to whether a person had lost teeth, regardless of. Smoking and drinking were also dichotomized into 'yes' or 'no.' Therefore, the referent group for these analyses was composed of persons who neither smoked tobacco, nor drank alcohol, nor had lost any teeth. As Table 8 shows, while smoking and drinking each carried a risk of oral cancer of approximately two-fold, inadequate dentition alone carried almost four times the risk of that of adequate dentition, with an OR of 3.9 ( ). When the joint effects of all three risk factors Table 5. Loss of teeth and the risk of oral cancer in females Risk factor Cases Controls ORc" ORa b 95 % CI No lost teeth Referent Lost with Lost without of lost teeth of lost teeth with of lost teeth without ~Crude OR. BOR adjusted by conditional logistic regression for tobacco smoking, alcohol drinking, years of education, gender, and age. 239

6 T. Zbeng et al. were examined, it was found that those who had all three (inadequate dentition, tobacco smoking, and alcohol drinking) carried a risk more than 15 times greater than those who had none of these risk factors. The possible association between oral cancer risk and the history of oral ulceration, X-ray or radiation exposure to the head or oral cavity, broken teeth, decayed teeth, septic teeth, filled teeth, and caries was also examined. None of these factors presented itself as a noteworthy risk factor. Discussion The findings of this study are consistent with several other recent epidemiologic studies which suggest that there is no association between oral cancer risk and the use of dentures, that there is an increased risk associated with an increased number of missing teeth, and a decreased risk associated with tooth brushing. We have shown that these associations are independent of use of tobacco and alcohol. Table 6. Tooth-brushing, and risk of oral cancer Cases Controls ORc a ORa b 95% CI Tooth-brushing Yes 208 No 40 Brushing times per day > Tooth-brushing Yes 134 No 22 Brushing times per day > MEN Referent Referent Linear trend test P = WOMEN Referent Referent Linear trend test P = 0.11 acrude OR. Table 7. Oral mucosal lesions and risk of oral cancer Cases Controls ORc a ORa b 95% CI MEN No lesions Leukoplakia Erythroplasia 2 0 ND - Lichen planus WOMEN No lesions Leukoplakia 9 0 ND ND Erythroplasia 4 0 ND ND Lichen planus 15 0 ND ND Referent acrude OR. ND, not determinable. 240

7 Oral cancer in China Table 8. Inadequate dentition, smoking, drinking, and the risk of oral cancer of Inadequate Alcohol Tobacco cases and dentition drinking smoking controls ORa a 95% CI Referent aor adjusted by conditional logistic regression for years of education, age, and gender. ( + ) risk factor present. ( - ) risk factor absent. The relative risks in our study suggest that the interaction between these three factors is much more than additive and is approximately multiplicative. All three of these factors lead to chronic trauma to and irritation of the oral mucosa and it is reasonable to suppose that this may be the underlying mechanism of all three associations. On the other hand, the possibility cannot be ruled out there is some other unidentified factor(s) whose action is facilitated by these variables. For the present, however, programs for the prevention of oral cancer should focus on all three of these factors--the prevention of tooth loss, heavy alcohol consumption, and tobacco use. References 1. Martin H, Pflueger OH. Cancer of the cheek (buccal mucosa). Arch Surg 1935; 30: Wynder EL, Bross IJ, Feldman R. A study of the etiology of factors in cancer of the mouth. Cancer 1957; 6: Graham S, Dayal H, Rohrer T, et al. Dentition, diet, tobacco and alcohol in the epidemiology of oral cancer. JNCI 1977; 59: Silverman S, Gorsky M, Lazada F. Oral leukoplakia and malignant transformation: a follow-up study of 257 patients. Cancer 1984; 53: Browne RM, Camsey MC, Waterhouse JAH. Etiological factors in oral squamous cell carcinoma. Community Dent Oral Epidemiol 1977; 5: Gupta PC, Mehta FS, Daftary DK, et al. Incidence rates of oral cancer and natural history of oral precancerous lesion in a 10-year follow-up study of India villagers. Community Dent Oral Epidemiol 1980; 8: Malaowalla AM, Silverman S, Mani NJ, et al. Oral cancer in industrial workers of Gujarat, India. A prevalence and follow-up study. Cancer 1976; 37: Silverman S, Bhargava R, Mani NJ, et al. Malignant transformation and natural history of oral leukoplakia in industrial workers in Gujarat, India. Cancer 1976; 38: Pindborg JJ, Joist O, Renstrup G, et al. Studies in oral leukoplakia: A preliminary report on the period prevalence of malignant transformation in leukoplakia based on a follow-up study of 248 patients. J Am Dent Assoc 1968; 78: Silverman S, Rosen RD. Observations on the clinical characteristics and natural history of oral leukoplakia. JAm Dent Assoc 1968; 76: Boyle P, Zheng T, Macfarlane GJ, et al. Etiology and epidemiology of head and neck cancer. Current Opinion in Oncology 1990; 2: Boyle P, Macfarlane GJ, McGinn R, et al. Epidemiology of head and neck cancer. In: De Vries N and Gluckman J, eds. Second Primary Cancers of Head and Neck. Heidelberg: Springer-Verlag, Zheng T, Boyle P, Hu H, etal. Cigarette smoking, alcohol consumption, and risk of oral cancer: a case-control study in Beijing, People's Republic of China. Cancer Causes and Control 1990; 1: World Health Organization. International Classification of Diseases, 9th Revision. Geneva: WHO, Mantel N, Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. JNCI 1959; 22: Breslow NE, Day NE. Statistical Methods in Cancer Research. Vol L The Analysis of Case-controI Studies. Lyon: International Agency for Research on Cancer, 1980; IARC Sci Pub 32: Marshall J, Graham S, Haughey BP. Smoking, alcohol, dentition and diet in the epidemiology of oral cancer. Submitted for publication. 18. Kabat GC, Hebert JR, Wynder EL. Risk factors for oral cancer in women. Cancer Res 1989; 49: Franco EL, Kowalski LP, Oliveira BV, et al. Risk factors for oral cancer in Brazil: a case-control study, lntj Cancer 1989; 43."

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