Cancer Risk and Diet in India
R Sinha1, DE Anderson2, SS McDonald2, P Greenwald3,
1 Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, 6120 Executive Boulevard, Executive Plaza South, Room 3046, Bethesda, Maryland, 20892-7273., USA
2 The Scientific Consulting Group, Inc., Gaithersburg, Maryland, USA
3 Division of Cancer Prevention, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, 20892-7273, USA
Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, 6120 Executive Boulevard, Executive Plaza South, Room 3046, Bethesda, Maryland, 20892-7273.
India is a developing country with one of the most diverse populations and diets in the world. Cancer rates in India are lower than those seen in Western countries, but are rising with increasing migration of rural population to the cities, increase in life expectancy and changes in lifestyles. In India, rates for oral and oesophageal cancers are some of the highest in the world. In contrast, the rates for colorectal, prostate, and lung cancers are one of the lowest. Studies of Indian immigrants in Western societies indicate that rates of cancer and other chronic diseases, such as coronary heart disease and diabetes, increase dramatically after a generation in the adopted country. Change of diet is among the factors that may be responsible for the changing disease rates. Diet in India encompasses diversity unknown to most other countries, with many dietary patterns emanating from cultural and religious teachings that have existed for thousands of years. Very little is known, however, about the role of the Indian diet in causation of cancer or its role, if any, in prevention of cancer, although more attention is being focused on certain aspects of the Indian diet, such as vegetarianism, spices, and food additives. Of particular interest for cancer prevention is the role of turmeric (curcumin), an ingredient in common Indian curry spice. Researchers also have investigated cumin, chilies, kalakhar, Amrita Bindu, and various plant seeds for their apparent cancer preventive properties. Few prospective studies, however, have been conducted to investigate the role of Indian diet and its various components in prevention of cancer. From a public health perspective, there is an increasing need to develop cancer prevention programs responsive to the unique diets and cultural practices of the people of India.
|How to cite this article:|
Sinha R, Anderson D E, McDonald S S, Greenwald P. Cancer Risk and Diet in India
.J Postgrad Med 2003;49:222-228
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Sinha R, Anderson D E, McDonald S S, Greenwald P. Cancer Risk and Diet in India
. J Postgrad Med [serial online] 2003 [cited 2019 Jun 17 ];49:222-228
Available from: http://www.jpgmonline.com/text.asp?2003/49/3/222/1138
The relationship between diet and health has been recognized throughout recorded history. Disease prevention through healthy preparation of foods and eating habits has been discussed in religious and civil writings for thousands of years. Since the 19th century, western scientific methodologies have been applied to the study of diet and disease with the intent of reducing the disease burden from non-communicable diseases (NCD) such as cancer, coronary heart disease (CHD), and other conditions endemic to societies after the advent of industrialization. Ecologic, observational, and laboratory studies generally agree that eating a diet high in vegetables, fruits, and other plant-based foods; low in animal fats and low in salt content, along with maintaining a healthy weight, not using tobacco in any form, and being physically active can reduce the risk of cancer, CHD, and other chronic diseases., Diet-related NCDs are of great concern to researchers assessing the impact of changes in diet in “developing” countries, such as India. Trends, based on current and projected data, in nutritional and disease status indicate that these countries face considerable challenges as under-nutrition evolves into over-nutrition as the community becomes “developed”.
India, a country in transition from a “developing” to a “developed” nation, is home to more than one billion people, with an ever-increasing middle class population with greater disposable incomes. Fourteen major languages and hundreds of dialects are spoken. Dietary customs and habits in India are diverse, owing in part, to the range of religions in the society, many of which provide specific dietary guidance for their followers. Furthermore, there is a tradition of linking vegetarianism with medicine. For example, Ayurveda provides dietary guidance and proscriptions that have been developed over millennia to prevent and treat multiple ailments, including CHD, cancer, and diabetes. Cancer rates in India are rising as development progresses, with a changing profile of burden at different cancer sites. According to the World Health Organization (WHO), cancer rates in India are considerably lower than those in more developed countries such as the United States (see [Table:1]). Data from population based cancer registries in India show that the most frequently reported cancer sites in males are lung, oesophagus,. stomach, and larynx. In females, cancers of the cervix, breast, ovary, and oesophagus are the most commonly encountered.
Contrary to what is seen in most developing countries, India has some of the highest CHD rates in the world, with urban rates being three times higher than rural rates. In addition, rates for obesity and diabetes are increasing dramatically in urban areas and in high-income rural residents., For example, the prevalence of diabetes in urban areas has been reported at 9-16%, more than four times the prevalence of two decades ago. Diet appears to be related to the high rates of CHD, obesity, and diabetes, although a genetic component may exist in some cases. In recent decades, consumption of foodgrains also has shifted from coarse grains (e.g., barley, rye, maize, millet, and sorghum) to refined rice and wheat.
Studies of immigrants provide insight into the contributions of environmental, behavioural, genetic, and lifestyle factors that determine risks for chronic diseases in Indians. Various immigration studies have included Asian Indians. Trends for cervical cancer incidence were investigated in a population-based study using 1968-1987 data from the Singapore Cancer Registry. Incidence rates were highest in women from India, followed by China and Malay. Data from 1968-1982 remained the same when compared in 5-year periods, although rates declined in each group. Data from the National Cancer Registry of Malaysia from 1987-1989 showed that site-specific cancers differ among Malays (larynx and oesophagus), Chinese (nasopharyngeal), and Indians (mouth cancers), and that Malaysia is in a cancer-transitional state from less industrialised (frequent sites: stomach, cervix, lung) to industrialised (frequent sites: lung, breast, rectum).
The Singapore Cardiovascular Cohort Study (SCCS) and the National University of Singapore Heart Study (NUSHS) investigated the relationship of risk factors for CHD and related conditions in Chinese and Indian immigrant populations and in indigenous Malays residing in the state. The NUSHS assessed dietary factors to determine the impact of diet on increasing rates of CHD, cerebrovascular disease, and cancer, and found vitamin C levels were lower in Malays and Asian Indians, which may have been responsible for higher CHD and cancer rates in those groups. The authors suggest that a low intake of fresh fruits and high cooking temperatures in Malay and Asian Indian dishes may account for the low levels of vitamin C. Recent case-control studies in Asian Indian immigrants in the United Kingdom and the United States identified high levels of homocysteine as a risk factor for the development of CHD, and cancer.
Dietary Factors And Lifestyle
India's rapid urbanization is characteristic of a country changing status from a “developing” to a “developed” country. Dietary changes, reductions in physical activity, and increasing obesity generally follow this transition, especially as urbanization occurs. Diet in India has been associated with the risk of chronic disease, although few of these associations have been investigated into or quantified adequately. Though not a comprehensive review, the following sections discuss factors of diet and lifestyle that may contribute to the growing burden of chronic diseases in India (summarized in [Table:2]).
Obesity and Physical Activity
Obesity and lack of physical activity are associated with increased risk at various cancer sites, including breast and endometrial cancer. In India, increases in the rates of obesity, central adiposity, and waist-hip ratio associated with urbanization are seen in every region and are highest among those with the highest levels of education and income. Energy balance, which includes maintaining ideal weight through physical exercise, has been associated with decreased risk of breast cancer. There are few large cross-sectional studies of energy balance in India. Among urban populations, energy intake has increased at the same time that energy expenditures have decreased, due in part to employment in industries reliant on mechanization. No comprehensive study of physical activity in India has been done, but small studies of selected populations suggest that levels of physical activity are inadequate to meet recommendations for prevention of chronic diseases.,
A large percentage of Indians, particularly Hindus, practice vegetarianism and avoid meat and fish products in their diet. Vegetarian diets have been associated with decreased risk for prostate cancer. Case-control studies that compared non-vegetarian and vegetarian diets and alcohol and tobacco use in India have reported that vegetarians have a reduced risk of oral, oesophageal, and breast cancers. Vegetarian diets rely on pulses (e.g., beans, chickpeas, and lentils) as a source of protein, and pulses have been significantly associated with reductions in cancer.,
Dietary Fats and Fiber
Diets high in saturated fats have been associated with increased risk for cancer. Fat intake, especially saturated fat, is increasing in the middle class in India, although some rural residents traditionally have had a high intake of ghee (clarified butter, high content of saturated fat), as well. Studies have given equivocal results regarding the link between fat intake and the risk of cancer., Large epidemiological studies have identified a possible association between increased dietary fibre and a decreased risk for cancers of the colon and breast. No large studies on dietary fibre have been conducted in India, and rates of colon and breast cancer are low compared to those in western societies. The Indian diet, which generally includes adequate levels of vegetables, fruits, and fiber-rich grains, may provide some protection against increased risk for these cancers.
Spices and Food Additives
Diet in India developed over thousands of years and is based on a mix of religious and secular beliefs. For example, Ayurveda medicine prescribes more than 700 plant-based medicines that contain spices and food additives to encourage good health. Many of these foodstuffs have been studied for their disease prevention capabilities, including turmeric (curcumin), cumin, chilies, kalakhar, Amrita Bindu, and various plant seeds. Among the most studied in recent years is turmeric, an ingredient in the common Indian curry and a spice that has been shown to be a potent antioxidant and anti-inflammatory agent with additional promise as a chemo-preventive agent. In a study in human blood cancer cell lines, turmeric suppressed and destroyed blood cancer cells. Turmeric has been shown to suppress tumour initiation, promotion, and metastasis in experimental studies. To illustrate, turmeric may block the activity of nuclear factor kappa-B (NfkB), which, in an activated state, appears to be associated with cancer cell growth in many cell types. Turmeric also has been found to inhibit the growth of 19 clinical strains of Helicobacter pylori, a carcinogenic bacterium linked to the increased risk of adenocarcinoma of the stomach and colorectal adenomas.
Amrita Bindu, a dietary supplement that is a salt-spice-herbal mixture, was found to protect rats against cancer induced by N-methyl-N-nitrosoguanidine, a potent carcinogenic nitrosamine. Possible mechanisms that explain the chemo-preventive role of Amrita Bindu include prevention of depletion of vitamins A, C, and E and of the anti-oxidant enzymes glutathione peroxidase and superoxide dismutase in the liver of rats. These actions in turn, prevent the rise of lipid peroxidation in the plasma and liver; and enhance glutathionine actions in both blood and liver.
A recent study investigated the anti-carcinogenic effectsof nine Indian spices on induction by dietary benzo[a] pyrene (B[a]P) of squamous cell carcinomas (SCC) of the stomach in mice and induction by dietary 3'-methyl-4-dimethylaminoazobenzene of hepatomas in rats. Cumin seeds and basil leaves significantly decreased the incidence of both SCC and hepatomas; poppy seeds significantly inhibited B[a]P-induced SCC; and the other six spices showed no effect.
Studies on spices and food additives have been conducted in vitro and in animal studies. Because of intriguing findings from these studies, there is a need to investigate these dietary factors in human studies.
Micronutrients play a significant role in maintaining health and preventing disease, including cancer, through a wide range of mechanisms: anti-oxidation, anti-proliferation, and repair of DNA damage. Direct and indirect relationships between micronutrients and health have been described in experimental, epidemiological and clinical trials. Vitamin deficiencies, specifically of vitamins A, C and E, may contribute to the high prevalence of oral cancers in India. A study carried out in rural India found that the presence of lesions was associated in patients with oral pre-cancerous lesions with low plasma levels of vitamins E and b-carotene. A study of Kurchias (a tribal population in Kerala, India, who consume a diet high in micronutrients and have a low prevalence of CHD and other chronic diseases of aging, including cancer) found that levels of serum vitamins A and E were inversely related to levels of lipid peroxides and CHD risk factors. Micronutrient deficiencies of iodine, iron, and vitamin A are highly prevalent in Indian children. Among 6-14-year-olds, goiter, caused by iodine deficiency and related to thyroid cancer, has a prevalence rate of 0.33 to 2.4%.
Dietary Guidance in India
For the past 70 years, the Indian Council of Medical Research (ICMR) has produced information on nutritional requirements specific to the population of India. Approximately every 10 years, the ICMR updates nutrition recommendations based on evolving information from surveys conducted by the National Institute of Nutrition (NIN), Hyberabad. The latest survey, completed in 2000, found that the Indian diet and nutrient intakes have hardly changed in the last 20 years. For cancer prevention, the NIN recommends a diet that includes high intake of fresh vegetables and fruits, with spices such as turmeric, in adequate amounts.
Incidence rates for oral cancer in India are among the highest in the world; most are associated with diet, weight, and other lifestyle factors. A significant lifestyle risk factor is betel quid (paan) chewing, a practice that is highly prevalent in India. Betel quid contains a variety of ingredients such as lime, catechu, and areca nut and is often mixed with tobacco. A case-control study in Southern India investigated the influence of paan, body mass index (BMI), diet, infections, and sexual practices on oral cancer. BMI was inversely associated with oral cancer, and paan chewers with low BMI had a very high risk of developing oral cancer. Frequent consumption of fish, eggs, a variety of raw and cooked vegetables, and fruit was associated with a decreased risk of oral cancer. A study on reverse smoking (i.e. smoking with the glowing end inside the mouth) revealed that use of tobacco in this form conferred a 5.19 times higher risk of oral pre-cancerous lesions of the palate than did use of chewing tobacco. Diets low in vegetables and fruits and high in alcohol increase the risk of oral cancers.
In India, the incidence of oesophageal cancer is moderately high and is associated with certain diets and lifestyles. Oesophageal cancer is the second most common cancer among males and the fourth most common cancer among females according to combined data from cancer registries in India. Among risk factors for oesophageal cancer in India, betel quid chewing carries a relative risk of 1.5 to 3.5. Salted tea, made by adding sodium bicarbonate, has shown high methylation activity and can result in endogenous formation of nitrosamines. Commonly used fresh and sun-dried vegetables and chilies also have a high content of nitrates or nitrosamines and may be associated with higher rates of oesophageal cancer. Various foods and food additives have been studied for their association with this disease. For example, kalakhar is a highly alkaline substance made from the charred false stem or from the skin of a particular variety of banana that is used as a coffee decoction or during the preparation of curry or “dal.” Daily use of kalakhar greatly increased the risk (OR=8.0) of oesophageal cancer. In the same study, spicy foods (OR=5.1) and chilies (OR=6.9) also resulted in a significantly increased risk. Another case-control study found alcohol (OR=7.81 with daily use), chewing betel leaf with tobacco (OR=3.16), bidi smoking (OR=1.95), and a diet low in vegetable consumption (OR=1.88) to be risk factors for oesophageal cancer.
Endometrial, Cervical, and Ovarian Cancers
Cancer of the female reproductive tract has a high incidence amongst Indian women. Human papilloma virus (HPV) is the most prevalent risk factor for cervical cancer and has been associated with cancer of the ovaries and endometrium. Environmental and dietary risk factors for cervical, ovarian, and endometrial cancers have been investigated in case-control and cohort studies. Cervical cancer is the most common cancer of the female genital tract in India, with approximately 100,000 new cases occurring each year. This accounts for almost 20% of all new cases diagnosed in the world annually. The incidence higher in rural areas, where prevention and screening programs are not as easily available as in urban areas., A review of studies on diet and cancers of the cervix, ovary, and endometrium have provided equivocal results. Some of the studies have suggested that a diet high in carotenoids, vegetables, and fruits may reduce the risk of cervical, ovarian, and endometrial cancers; high intake of vitamins C and E may reduce the risk of cervical cancer; and a diet high in fish may reduce the risk of ovarian cancer.
In India, the incidence of breast cancer is increasing, with an estimated 80,000 new cases diagnosed annually. The incidence of breast cancer increased by approximately 50% between 1965 and 1985. Much of this increase may be associated with greater urbanization and improved life expectancy. The incidence rates, education level, and income are higher in urban areas compared with rural areas. In addition, age at puberty and pregnancy-related factors, such as parity, age at giving birth to the first baby, and number of children, are factors possibly related to breast cancer. Few studies of diet and breast cancer in India have been published. The nutrition guidelines follow the World Cancer Research Fund recommendations that advocate having a diet containing vegetables and fruits in large amounts, reducing the intake of saturated fats, and increasing physical activity.
Compared to other countries, stomach cancer incidence rates are moderate to low in India, although certain populations, such as those in the Chennai area, have very high rates. A recent case-control study in Mumbai found that consumption of dried fish (OR=12.4) increased the risk while green tea consumption (OR=0.4) decreased the risk of having stomach cancer. A prospective case-control study from Trivandrum evaluated dietary risk factors for stomach cancer and found that high consumption of rice (OR=3.9), spicy food (OR=2.3), chili (OR=7.4), and high-temperature food (OR=7.0) increased the risk of developing stomach cancer. Fried foods are associated with higher rates of cancer due in part to the production of carcinogenic or mutagenic heterocyclic amines (HA) during the cooking process. Case-control and prospective studies have reported an increased risk of stomach (RR=2.5), colon (OR=2.7), and bladder (RR=2.6) cancers with moderate to heavy consumption of fried foods. Studies of mice fed with deep-fried vegetables and salted or sun-dried Ribbonfish, which is commonplace in Indian cooking, reported a 20 percent increase in gastric carcinoma. The rise has been attributed to the presence of polycyclic aromatic hydrocarbons produced by the cooking method. As mentioned earlier, the use of the spice turmeric is associated with a reduced risk of stomach cancer, in part because of its protective effect against the carcinogenic bacterium H. pylori, a major risk factor for stomach cancer.
Diet is an important factor in cancer aetiology and prevention in India. As a society, Indians have one of the most interesting diets, with many unique dietary constituents that have promise for cancer prevention. Very few well-designed, prospective epidemiological research studies exploring the relationships between diet and lifestyle and cancer have been carried out in India (see [Table:3]).
Additional research is needed to assess the impact of diverse dietary habits, religious practices, and lifestyles on prevention of cancer. Cancer detection and prevention efforts can have enormous benefits for developing countries by reducing future disease burden while saving economic resources for needed improvements in societal infrastructure. As development and mechanization continue into the 21st century, India must grapple with a transition from the burden of communicable diseases to the burden of NCDs.
|1||Ahmed S. Coronary heart disease: the Indian Asian diet. Nurs Stand 1999;13:45-7.|
|2||World Cancer Research Fund, American Institute for Cancer Research. Food, nutrition, and the prevention of cancer: a global perspective / World Cancer Research Fund, in association with American Institute for Cancer Research. Washington, DC: American Institute for Cancer Research, 1997.|
|3||Schaefer EJ. Lipoproteins, nutrition, and heart disease. Am J Clin Nutr 2002;75:191-212.|
|4||Popkin BM, Horton S, Kim S, Mahal A, Shuigao J. Trends in diet, nutritional status, and diet-related noncommunicable diseases in China and India: the economic costs of the nutrition transition. Nutr Rev 2001;59:379-90.|
|5||Fenley J, Bray F, Pisani DMe. World Health Organization. GLOBOCAN 2000: Cancer incidence, mortality and prevalence worldwide. Lyon, France: IARC Press; 2001. |
|6||Gajalakshmi V, Swaminathan R, Shanta V. An Independent Survey to Assess Completeness of Registration: Population Based Cancer Registry, Chennai, India. Asian Pac J Cancer Prev 2001;2:179-83.|
|7||Gopalan C. Rising incidence of obesity, coronary heart disease and diabetes in the Indian urban middle class. Possible role of genetic and environmental factors. World Rev Nutr Diet 2001;90:127-43.|
|8||Pradeepa R, Deepa R, Mohan V. Epidemiology of diabetes in India-current perspective and future projections. J Indian Med Assoc 2002;100:144-8.|
|9||Seow A, Chia KS, Lee HP. Cervical cancer: trends in incidence and mortality in Singapore 1968 to 1987. Ann Acad Med Singapore 1992;21:328-33.|
|10||Chan CK, Singh J, Rasid BK, Devaraj T. Penang cancer cases reported to the National Cancer Registry of Malaysia, 1987-1990: an epidemiological analysis. Med J Malaysia 1994;49:122-31.|
|11||Hughes K, New AL, Lee BL, Ong CN. Plasma vitamins A, C and E in the general population of Singapore, 1993 to 1995. Ann Acad Med Singapore 1998;27:149-53.|
|12||Chambers JC, Wander GS, Kooner JS. Homocysteine and coronary heart disease amongst Indian Asians. Indian Heart J 2000;52:S5-8.|
|13||Chandalia M, Abate N, Cabo-Chan AV Jr, Devaraj S, Jialal I, Grundy SM. Hyperhomocysteinemia in Asian Indians living in the United States. J Clin Endocrinol Metab 2003;88:1089-95.|
|14||Wu LL, Wu JT. Hyperhomocysteinemia is a risk factor for cancer and a new potential tumor marker. Clin Chim Acta 2002;322:21-8.|
|15||Misra A, Sharma R, Pandey RM, Khanna N. Adverse profile of dietary nutrients, anthropometry, and lipids in urban dwellers in Northern India. Eur J Clin Nutr 2001;55:727-34.|
|16||Bialostoslky K, et al. Dietary intake of macronutrients, micronutrients, and other dietary constituents: United States 1988-94. National Center for Health Statistics. Vital Health Stat 2002;11.|
|17||IARC Working Group on the Evaluation of Cancer-Preventive Strategies. In: Vanio H, Bianchini F, editors. IARC Handbooks of Cancer Prevention, Weight control and physical activity. Lyon, France: IARC Press; 2002. Vol. 6. |
|18||Shetty PS. Nutrition transition in India. Public Health Nutr 2002;5:175-82.|
|19||Kaur N, Mann SK, Sidhu P, Sangha JK. A comparative study of energy balance among housewives of Ludhiana city. Indian J Matern Child Health 1997;8:76-8.|
|20||Vaz M, Bharathi AV. Practices and perceptions of physical activity in urban, employed, middle-class Indians. Indian Heart J 2000;52:301-6.|
|21||Singh RB, Rastogi SS, Rao PV, Das S, Madhu SV, Das AK, et al. Diet and lifestyle guidelines and desirable levels of risk factors for the prevention of diabetes and its vascular complications in Indians: a scientific statement of The International College of Nutrition. Indian Consensus Group for the Prevention of Diabetes. J Cardiovasc Risk 1997;4:201-8.|
|22||Rajaram S, Sabate J. Health benefits of a vegetarian diet. Nutrition 2000;16:531-3.|
|23||Rao DN, Ganesh B, Rao RS, Desai PB. Risk assessment of tobacco, alcohol and diet in oral cancer-a case-control study. Int J Cancer 1994;58:469-73.|
|24||Rao DN. Role of vegetarian diet in cancers of the oesophagus and female breast in India. Vegetarian Congress Research Presentations, Section I: Diet and Chronic Disease. Loma Linda University Press; 1997. pp. 4, 2003. |
|25||Jain MG, Hislop GT, Howe GR, Ghadirian P. Plant foods, antioxidants, and prostate cancer risk: findings from case-control studies in Canada. Nutr Cancer 1999;34:173-84.|
|26||Mills PK, Beeson WL, Phillips RL, Fraser GE. Cohort study of diet, lifestyle, and prostate cancer in Adventist men. Cancer 1989;64:598-604.|
|27||Ghafoorunissa. Requirements of dietary fats to meet nutritional needs & prevent the risk of atherosclerosis-an Indian perspective. Indian J Med Res 1998;108:191-202.|
|28||Law M. Dietary fat and adult diseases and the implications for childhood nutrition: an epidemiologic approach. Am J Clin Nutr. 2000;72:1291S-6S.|
|29||Aggarwal BB, Kumar A, Bharti AC. Anticancer potential of curcumin: preclinical and clinical studies. Anticancer Res 2003;23:363-98.|
|30||Mahady GB, Pendland SL, Yun G, Lu ZZ. Turmeric (Curcuma longa) and curcumin inhibit the growth of Helicobacter pylori, a group 1 carcinogen. Anticancer Res 2002;22:4179-81.|
|31||Shanmugasundaram KR, Ramanujam S, Shanmugasundaram ER. Amrita Bindu-a salt-spice-herbal health food supplement for the prevention of nitrosamine induced depletion of antioxidants. J Ethnopharmacol 1994;42:83-93.|
|32||Aruna K, Sivaramakrishnan VM. Anticarcinogenic effects of some Indian plant products. Food Chem Toxicol 1992;30:953-6.|
|33||Tandon M, Kapil U, Bahadur S, Dwivedi SN, Pathak P. Role of micro-nutrients and trace elements in carcinoma of larynx. J Assoc Physicians India 2000;48:995-8.|
|34||Patel PS, Raval GN, Patel DD, Sainger RN, Shah MH, Shah JS, et al. A Study of Various Sociodemographic Factors and Plasma Vitamin Levels in Oral and Pharyngeal Cancer in Gujarat, India. Asian Pac J Cancer Prev 2001;2:215-24.|
|35||Reddy KK, Rao AP, Reddy TP. Serum vitamins E, A and lipid peroxidation levels in Kurichias, an Indian tribal population. Indian J Biochem Biophys 1999;36:44-50.|
|36||Chakravarty I, Ghosh K. Micronutrient malnutrition-present status and future remedies. J Indian Med Assoc 2000;98:539-42.|
|37||Vijayaraghavan K, Rao DH. Diet & nutrition situation in rural India. Indian J Med Res 1998;108:243-53.|
|38||Krishnaswamy K, Polasa K. Diet, nutrition & cancer-the Indian scenario. Indian J Med Res 1995;102:200-9.|
|39||Rajkumar T, Sridhar H, Balaram P, Vaccarella S, Gajalakshmi V, Nandakumar A et al. Oral cancer in Southern India: the influence of body size, diet, infections and sexual practices. Eur J Cancer Prev 2003;12:135-43.|
|40||Hebert JR, Gupta PC, Bhonsle RB, Mehta H, Zheng W, Sanderson M et al. Dietary exposures and oral precancerous lesions in Srikakulam District, Andhra Pradesh, India. Public Health Nutr 2002;5:303-12.|
|41||Malkan G, Mohandas KM. Epidemiology of digestive cancers in India. I. General principles and oesophageal cancer. Indian J Gastroenterol 1997;16:98-102.|
|42||Phukan RK, Chetia CK, Ali MS, Mahanta J. Role of dietary habits in the development of esophageal cancer in Assam, the north-eastern region of India. Nutr Cancer 2001;39:204-9.|
|43||Nayar D, Kapil U, Joshi YK, Sundaram KR, Srivastava SP, Shukla NK, et al. Nutritional risk factors in esophageal cancer. J Assoc Physicians India 2000;48:781-7.|
|44||Hisada M, van den Berg BJ, Strickler HD, Christianson RE, Wright WE, Waters DJ et al. Prospective study of antibody to human papilloma virus type 16 and risk of cervical, endometrial, and ovarian cancers (United States). Cancer Causes Control 2001:12:335-41.|
|45||Ghim SJ, Basu PS, Jenson A. Cervical cancer: etiology, pathogenesis, treatment, and future vaccines. Asian Pac J Cancer Prev 2002;3:207-14.|
|46||Radhakrishna Pillai M, Sreevidya S, Pollock BH, Jayaprakash PG, Herman B. Human papillomavirus type 16 E6 and E7 gene variations in Indian cervical cancer. Gynecol Oncol 2002;87:268-73.|
|47||Duttagupta C, Sengupta S, Roy M, Sengupta D, Chakraborty S, Bhattacharya P et al. Oncogenic human papillomavirus (HPV) infection and uterine cervical cancer: a screening strategy in the perspective of rural India. Eur J Cancer Prev 2002;11:447-56.|
|48||Potischman N, Brinton LA. Nutrition and cervical neoplasia. Cancer Causes Control 1996;7:113-26.|
|49||Bosetti C, Altieri A, La Vecchia C. Diet and environmental carcinogenesis in breast/gynaecological cancers. Curr Opin Obstet Gynecol 2002;14:13-8.|
|50||Saxena S, Szabo CI, Chopin S, Barjhoux L, Sinilnikova O, Lenoir G et al. BRCA1 and BRCA2 in Indian breast cancer patients. Hum Mutat 2002;20:473-4.|
|51||Singh MM, Devi R, Walia I, Kumar R. Breast self examination for early detection of breast cancer. Indian J Med Sci 1999;53:120-6.|
|52||Rao DN, Ganesh B, Dinshaw KA, Mohandas KM. A case-control study of stomach cancer in Mumbai, India. Int J Cancer 2002;99:727-31.|
|53||Mathew A, Gangadharan P, Varghese C, Nair MK. Diet and stomach cancer: a case-control study in South India. Eur J Cancer Prev 2000;9:89-97.|
|54||Balachandran B, Sivaramkrishnan VM. Induction of tumours by Indian dietary constituents. Indian J Cancer 1995;32:104-9.|
|55||Wu-Williams AH, Yu MC, Mack TM. Life-style, workplace, and stomach cancer by subsite in young men of Los Angeles County. Cancer Res 1990;50:2569-76.|
|56||Gerhardsson de Verdier M, Hagman U, Peters RK, Steineck G, Overvik E. Meat, cooking methods and colorectal cancer: a case-referent study in Stockholm. Int J Cancer 1991;49:520-5.|
|57||Chyou PH, Nomura AM, Stemmermann GN, Kato I. Lung cancer: a prospective study of smoking, occupation, and nutrient intake. Arch Environ Health 1993;48:69-72.|