INTRODUCTION
Betel quid contains the areca nut (fruit of the Areca catechu Linn.), a tropical plant. Chewing this is therefore a very popular pastime in some tropic areas, such as the Solomon Islands, Papua New Guinea, Palau, Southeast Asia, south India, and Taiwan. It is chewed by ∼600 million people (∼10% of the world’s population),1 but the extent of habits varies markedly from one region to another. Historically, the habits of betel quid chewing have been thriving for many decades and in countries, although the composition of the betel quid used varies with geography. In Papua New Guinea, prevalence has varied from 26.8% to 88.4% in different areas.2 It is estimated that 76.1% of the Palau’s population chewed betel quid.3 In India, a total of 33.0% reported chewing betel quid in all forms.4 A large scale study in Sri Lanka reported 50% of men and women to be chewing betel quid! Among the Taiwanese aborigines, 46.1% were reported to be betel quid chewers.5
Chewing betel quid is a popular habit in the Solomon Islands. During betel quid chewing, lime (calcium hydroxide made by burning coral) is added to the acidic betel nut (not the whole fruit) to reduce the astringent taste.6 It is an ancient practice enjoyed by islanders of both sexes that provides mild stimulation and a sweetening of the breath. The International Agency for Research on Cancer (IARC) declared in 2004 that chewing of betel quid without tobacco is carcinogenic to humans (Group 1). Epidemiologic studies also showed chewing betel quid contributed independently to the risk of oral and pharyngeal cancer7–9 and oral precancerous lesions.10,11
Oral and pharyngeal cancer is one of most common cancers in the Solomon Islands.12 In 2002, the age-standardized incidence rate for oral and pharynx cancer in the Solomon Islands was 37.0 per 100,000 for men and 22.5 per 100,000 for women.13 The age-standardized mortality rate of oral and pharynx cancer in 2002 was 21.0 per 100,000 for men and 13.0 per 100,000 for women.13 A high proportion of oral and pharynx cancer highlights the public health problems of betel quid chewing in the Solomon Islands. Limited data have been published on betel quid prevalence in the Solomon Islands, where oral cancer is highly endemic, and so the purpose of this study is to provide the first description of betel chewing prevalence and an analysis of the sociodemographic factors related to it in the Solomon Islands.
MATERIALS AND METHODS
Study population.
The population of Solomon Islands is ∼500,000, with a total land mass of 28,450 km2; the capital is Honiara. The island’s nine provinces lack a household registry system, and combined with traffic inconveniences, random sampling by door-to-door or telephone questionnaire methods was difficult. Therefore, we randomly selected 35 healthy persons whose relatives attended health stations in each province. Each participant completed an interview questionnaire with trained nurses and physicians, fulfilling our target population of 315 persons. The prevalence of betel quid use and its related sociodemographic factors among the Solomon Islands was compiled. Data were obtained by interviewing participants in their communities in 2005. Questionnaire contents included demographic characteristics, body morphology (height and weight), past and current histories of betel chewing, and cigarette and alcohol use. The study was approved by Human Ethics Committee, National Health Research Institutes of Taiwan and Ministry of Health and Medical Services Ethics and Research Committee of Solomon islands, and all participants signed informed consent forms.
Data analysis.
Dependent variables.
Data were analyzed for sociodemographic factors associated with betel quid chewing. The dichotomous dependent variable, betel quid chewing behavior, was coded as betel quid chewers (chewed at least once a week, irrespective of quantity) or never chewers (those who never chewed). Smoking and drinking behaviors were coded as smokers/drinkers (smoked/drank least once a week, irrespective of quantity) or never smokers/drinkers (those who never smoked/drank).
Independent variables.
Potential explanatory (independent) variables included sex, age group, marital status, religion, education levels, occupation, obesity, cigarette smoking, and alcohol consumption. Body mass index (BMI) was calculated (BMI = weight/height2 [kg/m2]). Obesity was defined as BMI ≥ 27.8 kg/m2 for men and ≥ 27.3 kg/m2 for women.
Statistical analyses.
Data were entered into a spreadsheet and analyzed using Statistic Analysis Software (SAS release 9.1; SAS Institute, Cary, NC). Missing data were excluded. Crude odds ratios (ORs) with 95% CI were calculated. To control for potential confounding effects, statistically significant ORs were subsequently examined in the multiple logistic regression model to obtain adjusted ORs (aORs). P < 0.05 or a range of 95% CI not including unity were considered statistically significant.
RESULTS
A total of 315 participants completed our questionnaires from the Solomon Islands. The sociodemographic survey is shown in Table 1. The prevalence of betel quid chewers was 76.8% (83% for men and 68% for women). Prevalence of cigarette smoking was 53.0% and prevalence of alcohol use was 36.8%. Table 1 depicts the distribution of the sociodemographic characteristics comparing betel quid chewers to never chewers. In the adjusted analysis, the OR showed those who were smokers to be more likely to be betel quid chewers (OR = 3.95, 95% CI = 1.87–8.33). It was noteworthy that the aOR stratified by religion showed that Seventh-Day Adventists were less likely to have chewing habits (OR = 0.08, 95% CI = 0.04–0.18). The habits of betel quid use were evaluated in Table 2. Men chewed significantly higher amounts of quid (13.2 ± 32.8) per day than women (4.8 ± 4.8; P < 0.01). As seen in Table 2, there was a noticeable difference in the starting age for quid chewing: in the young generation, men started at 13.2 years and women at 14.7 years old, whereas the older generation had started later at 18.8 and 18.2 years old, respectively (P < 0.01). In both women and men, there is now a trend to start quid chewing at earlier ages. In addition, the older age group had a significantly longer chewing time than the younger age group.
DISCUSSION
In the Solomon Islands, research into the prevalence of betel quid chewing and its related sociodemographic factors is limited. In this survey, the socio-demographic factors in chewing behavior were examined. Compared with never chewers, betel quid chewers were more likely to be smokers.
Betel quid chewing behavior.
Betel quid is used by ∼10% of the world’s population,1 and the chewing habits are mostly concentrated in Southeast Asia (India, Sri Lanka, Pakistan, Taiwan, Cambodia, Myanmar, Malaysia, and Thailand), and the Pacific islands (Solomon Islands, Palau, and Papua New Guinea). The overall age-standardized incidence rate adjusted by world population (ASRW) for oral and pharyngeal cancers in the world in 2002 was 10.1 per 100,000 for men and 4.0 per 100,000 for women.13
The prevalence of betel quid chewing by country and the occurrence of oral and pharynx cancer is shown in Table 3. Although it is difficult to combine chewing prevalence with the incidence of oral and pharyngeal cancer, we still can observe a trend between chewing prevalence and the incidence of oral and pharyngeal cancer by different countries. A high incidence of oral and pharyngeal cancer is observed in some countries where a high proportion of the population chews betel quid. In the Solomon Islands, the ASRW of oral and pharyngeal cancer was 37.0 per 100,000 in men and 22.5 per 100,000 in women. The highest prevalence of betel quid chewing was also present in the Solomon Islands, and its oral cancer incidence ranked second in the world. In Papua New Guinea, the incidence for oral cancer in men was 41.2 per 100,000 and 26.9 per 100,000 in women, making it first in the world. The prevalence of betel quid chewing was also higher (57.7%) in Papua New Guinea.14 However, relevant Papua New Guinea statistics dates from nearly 40 years ago and perhaps this needs to be re-explored. In a large-scale epidemiology study of Sri Lanka, the reported prevalence of betel quid chewing was 45.2%,15 with the incidence of oral and pharyngeal cancer being higher in Sri Lanka.13
India has the largest betel quid–consuming population in the world. In a large-scale survey in Mumbai (Bombay), India, 33.0% reported chewing betel quid in all forms. The prevalence of oral cancer was also noted to be high in India.13 Similarly, in Karachi of Pakistan, there is a high prevalence of betel quid chewing and also a high prevalence of oral cancer.16 Oral cancer is also prevalent in Taiwan, particularly in men, where the age-adjusted incidence rate was 27.4 per 100,000.17 Correspondingly, the prevalence of betel quid chewers was 16.5% in men.
In Mainland China, the habit of betel quid chewing is common in the provinces of Hunan, Hainan, and Yunnan. A large-scale study in Xiangtan city, Hunan Province, was designed to explore the association between oral submucous fibrosis (OSF) and betel quid chewing. In a total of 11,046 subjects, 35.4% subjects had a habit of betel quid chewing, of which 39.4% were men and 30.5% were women.18 Of the participants, 335 (3.0%) subjects were diagnosed with OSF.18
The intermediate prevalence of betel quid chewing may lead to intermediate oral cancer incidence rate in some countries, such as Cambodia, Myanmar, Malaysia,2 and Thailand.2,13,19 Betel quid chewing is prevalent, mainly among elderly Cambodian women.20 In the Myanmar population, 16.2% were regular betel quid chewers,21 and the incidence of oral and pharyngeal cancer was estimated to be 16.3 per 100,000 in men and 5.3 per 100,000 in women.13 Among Malay people, the prevalence of current betel quid chewers was 18.4%.2 The ASRW of oral and pharyngeal cancer in 2002 was 5.3 per 100,000 for Malay men and 3.4 per 100,000 for Malay women.13 In Thailand, a prevalence study of precancerous and oral mucosal lesions in 1,866 subjects (986 men and 880 women) showed that 17.3% were betel-quid chewers, with a prevalence of 15.8% in men and 18.9% in women.19 Chewing betel quid was more prevalent for older people; the chewing habits had been given up among younger people.22 Corresponding, betel quid chewing is declining in Thailand, the only country in southeast Asia to present such a trend.1 Changes of traditional chewing habits among Thais are associated with a marked decrease of oral cancer incidence between 1988 and 1999.22 In 2002, the ASRW of oral and pharyngeal cancer was only 7.2 per 100,000 in men and 4.6 per 100,000 in women.13
According to the GLOBOCAN 2002 database, a lower incidence of oral and pharyngeal cancer was found in some countries, such as Japan (men: 5.0/100,000; women: 2.2/ 100,000), Singapore (men: 6.2/100,000; women: 2.6/100,000), Canada (men: 9.6/100,000; women: 3.7/100,000), the United States (men: 12.2/100,000; women: 4.3/100,000), and the United Kingdom (men: 7.5/100,000; women: 3.5/100,000). The oral and pharyngeal cancer occurrences in the general population might be caused by alcohol or cigarette use, but the issue of betel quid use among immigrants needs to mentioned.2 There were discrepancy habits of betel quid use between migrants and the general population.23 In Japan, Singapore, Canada, the United States, and the United Kingdom, the general population does not chew betel quid, but there are groups of migrants who do chew betel quid. In Singapore, the habit of betel quid chewing is continued by older Indian people and Malay women.2 Indeed, in the Indian community of Singapore, 6.4% of participants reported the tradition of betel quid chewing.2 In Canada, the United States, and the United Kingdom, betel quid use is prevalent in Asian migrants, and the chewing patterns are very similar to their countries of origin.2,23 A migrant study also confirmed that the general population from Asia (India, Pakistan, Bangladesh, Nepal, and Sri Lanka) had a significantly higher percentage of oral cancer compared with others in southern England, providing an evidence of lifestyle habits, such as betel quid chewing.24 In Egypt, the lowest incidence (men: 0.9/ 100,000; women: 0.3/100,000) of oral cancer incidence might be caused by hardly any substance (alcohol, cigarettes, and betel quid) use in their people. Therefore, in most areas, the chewing of betel quid is an effect modifier or causes interactions with alcohol or cigarette use to cause oral and pharyngeal cancer, but in endemic areas, there is an association suggested by the higher prevalence of quid chewing and oral and pharyngeal cancer.
The Solomon Islands is a hyperendemic area for betel quid chewing, and chewing habits are a known risk factor for oral and pharyngeal cancer7–9 or oral precancerous disease.10,11 The Solomon Islands study has shown that the combination of smoking and betel quid chewing are the important risk factors for oral cancer.25 In our Solomon Islands study, the prevalence of betel quid chewing is ∼77% in the general population; of the quid chewers, 61.6% also smoked cigarettes. Clearly, the highest prevalence of betel quid chewing is strongly associated with oral cancer occurrences, and cigarette smoking enhances oral cancer development.7
In the Solomon Islands, betel quid chewing is a popular habit; chewing is common in both men and women. There were more men (83%) with chewing habits than women (68%) in this study. Likewise, in a study of Taiwan aborigines, men were more likely to become betel quid chewers than women.5 After adjusting for other factors, the prevalence of smoking habits was significantly higher in betel quid chewers than in those who never chewed. In terms of betel quid chewing habits, men chewed significantly higher amount of quids (13.2 ± 32.8) than women (4.8 ± 4.8). In the Solomon Islands, subjects who chewed higher amounts (> 5) of betel quid per day showed significantly higher risks of oral and pharyngeal cancer than those who chewed less quids (< 5).25 Also, note is made of a trend toward chewing betel quid at earlier ages in recent times. Therefore, education about betel quid chewing should be emphasized in the public prevention education of oral cancer in the Solomon Islands. Another important finding is that betel quid chewing is closely associated with religion. Seventh-Day Adventist subjects were less likely to be betel quid chewers. This might be explained by the abstinence from betel quid use in Seventh-Day Adventists.
In conclusion, betel quid chewing in the Solomon Islands is the most prevalent in the world over the last few years. Betel quid use is strongly associated with smoking and religion. Efforts to reduce habitual betel quid consumption and smoking might be of benefit in reduction of oral cancer incidence.
Sociodemographic characteristics and betel quid chewing behaviors in the Solomon Islands (N = 315), 2005
| Betel quid chewers(N 3242) | Never chewers(N 373) | |||
|---|---|---|---|---|
| Characteristics | [N (%)] | [N (%)] | OR* (95% CI) | aOR† (95% CI) |
| * Odds ratios (OR) refer to risk of betel quid chewers versus never chewers according to each variable. OR > 1 indicates a higher likelihood of being a betel quid chewer. | ||||
| † aOR, adjusted odds ratio for sex, religion, cigarette smoking, and alcohol drinking by logistic regression model; 95% CI: 95% confidence interval. | ||||
| ‡Significant difference in prevalence of betel quid chewing by χ2 analysis (P < 0.05). | ||||
| §Significant difference by logistic regression model (P < 0.05). | ||||
| Sex‡ | ||||
| Males | 151 (83) | 31 (17) | 2.25 (1.32–3.83)§ | 1.94 (0.95–3.97) |
| Females | 91 (68) | 42 (32) | 1.00 | 1.00 |
| Age group (years) | ||||
| ≤ 29 | 147 (79) | 39 (21) | 1.35 (0.80–2.29) | – |
| > 29 | 95 (74) | 34 (26) | 1.00 | – |
| Marital status | ||||
| Single | 109 (81) | 26 (19) | 1.48 (0.86–2.55) | – |
| Married | 133 (74) | 47 (26) | 1.00 | – |
| Religion‡ | ||||
| Seventh-Day Adventist | 26 (45) | 32 (55) | 0.15 (0.08–0.29)§ | 0.08 (0.04–0.18)§ |
| Others | 216 (84) | 41 (16) | 1.00 | |
| Education (years) | ||||
| > 6 | 147 (76) | 47 (24) | 0.81 (0.46–1.42) | – |
| ≤ 6 | 89 (79) | 23 (21) | 1.00 | – |
| Occupation | ||||
| Yes | 54 (72) | 21 (28) | 0.71 (0.39–1.28) | – |
| No | 188 (78) | 52 (22) | 1.00 | – |
| Obesity | ||||
| Yes | 51 (74) | 18 (26) | 0.82 (0.44–1.51) | – |
| No | 191 (78) | 55 (22) | 1.00 | – |
| Cigarette smoking‡ | ||||
| Yes | 149 (89) | 18 (11) | 4.68 (2.58–8.49)§ | 3.95 (1.87–8.33)§ |
| No | 92 (64) | 52 (36) | 1.00 | 1.00 |
| Alcohol drinking‡ | ||||
| Yes | 100 (86) | 16 (14) | 2.50 (1.35–4.62)§ | 2.14 (0.90–5.07) |
| No | 135 (71) | 54 (29) | 1.00 | 1.00 |
Age started chewing (years), quantities (a day), and duration (years) of betel quid chewers among Solomon Islands people (N = 217), 2005
| Men (N = 141) | Women (N = 76) | |||||
|---|---|---|---|---|---|---|
| Variable | Age ≤ 29 | Age > 29 | Total | Age ≤ 29 | Age > 29 | Total |
| * Significance difference between younger age group and older age group using two-sample independent t test (P < 0.01). | ||||||
| † Significance difference between men and women using two-sample independent t test (P < 0.01). | ||||||
| Age started chewing (years) | ||||||
| Mean ± SD | 13.2 ± 4.6 | 18.8 ± 6.3* | 15.6 ± 6.1 | 14.7 ± 4.3 | 18.2 ± 5.1* | 16.0 ± 4.9 |
| Range | 5–24 | 5–35 | 5–35 | 5–24 | 8–30 | 5–30 |
| Quids per day | ||||||
| Mean ± SD | 14.1 ± 35.6 | 11.9 ± 28.6 | 13.2 ± 32.8† | 4.5 ± 4.8 | 5.2 ± 4.9 | 4.8 ± 4.8 |
| Range | 1–294 | 0.5–210 | 0.5–294 | 0.5–20 | 1–15 | 0.5–20 |
| Chewing year | ||||||
| Mean ± SD | 9.6 ± 5.3 | 20.6 ± 9.8* | 14.2 ± 9.2 | 8.2 ± 4.4 | 21.0 ± 12.2* | 12.9 ± 10.2 |
| Range | 1–21 | 2–54 | 1–54 | 2–17 | 9–57 | 2–57 |
Prevalence of betel quid chewing among adults and their oral and pharynx incidence* in selected countries
| Prevalence of chewing† | Incidence‡ of oral and pharynx cancer | |||||
|---|---|---|---|---|---|---|
| Country | Reference | Men (%) | Women (%) | Total (%) | Men | Women |
| * From Ferlay and others (2003) GLOBOCAN 2002.13 | ||||||
| † From IARC report. | ||||||
| ‡ The age-standardized rates per 100,000 (standardized to the world standard population). | ||||||
| § From Department of Health, Taiwan, 2002.17 | ||||||
| Solomon Islands | Present | 83.0 | 68.4 | 76.8 | 37.0 | 22.5 |
| Palau | 3 | 72.0 | 80.0 | – | – | – |
| Papua New Guinea | 14 | 62.8 | 52.8 | 57.7 | 42.2 | 26.9 |
| Sri Lanka | 15 | 54.0 | 42.0 | 45.2 | 31.4 | 11.1 |
| China, Hunan province, Xiangtan city | 18 | 39.4 | 30.5 | 35.4 | – | – |
| India, Mumbai (Bombay) | 4 | 37.8 | 29.7 | 33.0 | 22.4 | 9.3 |
| Pakistan, Karachi | 16 | 27.9 | 37.8 | 32.5 | 21.4 | 17.3 |
| Taiwan | 26 | 16.5 | 2.9 | 10.0 | 27.4§ | 2.9§ |
| Cambodia | 27 | 6.8 | 40.6 | 31.2 | 14.6 | 4.2 |
| Myanmar | 21 | – | – | 16.2 | 16.3 | 5.3 |
| World | 1 | – | – | – | 10.1 | 4.0 |
Address correspondence to Ying-Chin Ko, Department of Public Health, Faculty of Medicine, College of Medicine, Kaohsiung Medical University, No. 100, Shih-Chuan 1st Road, Kaohsiung City, Taiwan. E-mail: ycko@nhri.org.tw
Authors’ addresses: Silent Tovosia, National Referral Hospital, Ministry of Health and Medical Services, the Solomon Islands. Ping-Ho Chen, Pei-Chien Tsai, and Ying-Chin Ko, Division of Environmental Health and Occupational Medicine, National Health Research Institutes, Kaohsiung, Taiwan. Allen Min-Jen Ko3, Liverpool Hospital, Sydney, Australia. Hung-Pin Tu, and Ying-Chin Ko, Department of Public Health, Faculty of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
Financial support: This study was supported by Grant NHRI-EO–095–PP–08 from the National Health Research Institutes.
REFERENCES
- 2↑
IARC, 2004. Betel-quid and areca-nut chewing and some areca-nut-derived nitrosamines. IARC Monogr Eval Carcinog Risks Hum 85 :52–77.
- 3↑
Ysaol J, Chilton JI, Callaghan P, 1996. A survey of betel nut chewing in Palau. Isla J Micrones Stud 4 :244–255.
- 4↑
Gupta PC, 1996. Survey of sociodemographic characteristics of tobacco use among 99,598 individuals in Bombay, India using handheld computers. Tob Control 5 :114–120.
- 5↑
Lin CF, Wang JD, Chen PH, Chang SJ, Yang YH, Ko YC, 2006. Predictors of betel quid chewing behavior and cessation patterns in Taiwan aborigines. BMC Public Health 6 :271.
- 6↑
Baker M, Le Mesurier R, Szetu J, Painter G, Hue J, McLellan S, Aluta W, 2006. Ocular trauma in the Solomon Islands. Clin Experiment Ophthalmol 34 :813–814.
- 7↑
Ko YC, Huang YL, Lee CH, Chen MJ, Lin LM, Tsai CC, 1995. Betel quid chewing, cigarette smoking and alcohol consumption related to oral cancer in Taiwan. J Oral Pathol Med 24 :450–453.
- 8
Lu CT, Yen YY, Ho CS, Ko YC, Tsai CC, Hsieh CC, Lan SJ, 1996. A case-control study of oral cancer in Changhua County, Taiwan. J Oral Pathol Med 25 :245–248.
- 9↑
Lee KW, Kuo WR, Tsai SM, Wu DC, Wang WM, Fang FM, Chiang FY, Ho KY, Wang LF, Tai CF, Kao EL, Chou SH, Lee CH, Chai CY, Ko YC, 2005. Different impact from betel quid, alcohol and cigarette: risk factors for pharyngeal and laryngeal cancer. Int J Cancer 117 :831–836.
- 10↑
Lee CH, Ko YC, Huang HL, Chao YY, Tsai CC, Shieh TY, Lin LM, 2003. The precancer risk of betel quid chewing, tobacco use and alcohol consumption in oral leukoplakia and oral submucous fibrosis in southern Taiwan. Br J Cancer 88 :366–372.
- 11↑
Yang YH, Lee HY, Tung S, Shieh TY, 2001. Epidemiological survey of oral submucous fibrosis and leukoplakia in aborigines of Taiwan. J Oral Pathol Med 30 :213–219.
- 12↑
Taylor R, Parker M, Ansford A, Davison A, 1983. Cancer in Solomon Islands 1970–82. P N G Med J 26 :102–110.
- 13↑
Ferlay J, Bray F, Pisani P, Parkin DM, 2003. Globocan 2002, Cancer Incidence, Mortality and Prevalence Worldwide. Lyon, France: IARC
- 14↑
Pindborg JJ, Barmes D, Roed-Petersen B, 1968. Epidemiology and histology of oral leukoplakia and leukoedema among Papuans and New Guineans. Cancer 22 :379–384.
- 15↑
Warnakulasuriya KAAS, 1992. Smoking and chewing habits in Sri Lanka: implications for oral cancer and precancer. Gupta PC, Hamner JE, Murtu PR, eds. Control of Tobacco-Related Cancers and Other Diseases. Bombay: Oxford University Press, 113–118.
- 16↑
Mahmood Z, Jaferey NA, Samiuddin M, Malik S, Qureshi SA, 1974. Dietary and other habits of people of Karachi. J Parkistan Med Assoc 26 :222–229.
- 17↑
Department of Health, Taiwan, 2002. Cancer Registration System Annual Report. Taipei, Taiwan: Bureau of Health Promotion, Department of Health.
- 18↑
Tang JG, Jian XF, Gao ML, Ling TY, Zhang KH, 1997. Epidemiological survey of oral submucous fibrosis in Xiangtan City, Hunan Province, China. Community Dent Oral Epidemiol 25 :177–180.
- 19↑
Reichart PA, Mohr U, Srisuwan S, Geerlings H, Theetranont C, Kangwanpong T, 1987. Precancerous and other oral mucosal lesions related to chewing, smoking and drinking habits in Thailand. Community Dent Oral Epidemiol 15 :152–160.
- 20↑
Reichart PA, Schmidtberg W, Scheifele C, 1996, Betel chewer’s mucosa in elderly Cambodian women. J Oral Pathol Med 25: 367–370.
- 21↑
Reichart PA, Way TH, 2006. Oral cancer and pre-cancer in Myanmar: a short review. J Oral Pathol Med 35 :193–196.
- 22↑
Reichart PA, Dietrich T, Khongkhunthian P, Srisuwan S, 2003. Decline of oropharyngeal cancer in Chiangmai province, Thailand, between 1988 and 1999. Oral Oncol 39 :569–573.
- 23↑
Warnakulasuriya S, 2002. Areca nut use following migration and its consequences. Addict Biol 7 :127–132.
- 24↑
Warnakulasuriya KAAS, Johnson NW, Linklater KM, Bell J, 1999. Cancer of mouth, pharynx and nasopharynx in Asian and Chinese immigrants resident in Thames regions. Oral Oncol 35 :471–475.
- 25↑
Lumukana R, King T, 2003. Smoking and chewing habits of oral cancer patients in the Solomon Islands. Pac Health Dialog 10 :41–44.
- 26
Ko YC, Chiang TA, Chang SJ, Hsieh SF, 1992. Prevalence of betel quid chewing habit in Taiwan and related sociodemographic factors. J Oral Pathol Med 21 :261–264.
- 27
Ikeda N, Handa Y, Khim SP, Durward C, Axell T, Mizuno T, Fukano H, Kawai T, 1995. Prevalence study of oral mucosal lesions in a selected Cambodian population. Community Dent Oral Epidemiol 23 :49–54.