IJC International Journal of Cancer

Salt tea consumption and esophageal cancer: A possible role of alkaline beverages in esophageal carcinogenesis Nazir Ahmad Dar1, Gulzar Ahmad Bhat1, Idrees Ayoub Shah1, Beenish Iqbal1, Rumaisa Rafiq1, Sumaiya Nabi1, Mohd Maqbool Lone2, Farhad Islami3,4 and Paolo Boffetta3 1

Department of Biochemistry, University of Kashmir, Hazratbal, Srinagar, Jammu and Kashmir, India Department of Radiation Oncology, SK Institute of Medical Sciences, Soura, Srinagar, Jammu and Kashmir, India 3 The Tisch Cancer Institute and Institute for Transitional Epidemiology, Mount Sinai School of Medicine, New York, NY 4 Digestive Disease Research Center, Shariati Hospital, Tehran University of Medical Sciences, Tehran, Iran 2

Esophageal cancer is the eighth most frequent malignancy worldwide, and the sixth most common cause of death from cancers.1 Esophageal squamous cell carcinoma (ESCC) is the most common histological type of esophageal cancer in lowand middle-income countries2 and constitutes 90% of the cases in the Asian “esophageal cancer belt.”2–4 Kashmir Valley in Jammu and Kashmir State, the northern most state of Key words: esophageal cancer, alkaline salt tea, cereal paste, samovar, Kashmir Additional Supporting Information may be found in the online version of this article. Group authorship information: NAD and PB designed the study. NAD executed the study and MML and GAB, IAS, BI, RR, and SN were involved in recruitment of subjects, data collection, and database development. NAD, FI, and PB, analyzed and interpreted the data. NAD drafted the manuscript. All authors reviewed the manuscript and approved the final version. Grant sponsor: Extramural grant of Indian Council of Medical Research (ICMR), New Delhi; Grant number: IRIS ID 5/13/37/ 2007/-NCD-III; Grant sponsor: Union for International Cancer Control (UICC). DOI: 10.1002/ijc.29204 History: Received 13 May 2014; Accepted 21 Aug 2014; Online 10 Sep 2014 Correspondence to: Nazir Ahmad Dar, Department of Biochemistry, University of Kashmir, Hazratbal Srinagar, Jammu and Kashmir, India 190006, E-mail: [email protected]

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India, lies in the cancer belt. Esophageal cancer is the most common cancer in Kashmir.5–7 The annual age adjusted incidence rate for esophageal cancer in Kashmir is 43.6 and 27.9 per 105 persons in males and females, respectively.6 Although several risk factors have been suggested, including hookah smoking and nass chewing,8 oral hygiene,9 animal contact,10 low socioeconomic status,11 major factors contributing to ESCC in Kashmir are yet to be established. Salt tea, a traditional beverage (locally called Noon Chai or Sheer Chai), is the most commonly used beverage in Kashmir. In contrast to some other risk factors, such as nass chewing, which may affect only a section of the general population or may have unequal distribution among males and females, salt tea drinking in Kashmir is widespread in both sexes and across all economic groups. In addition, consumption of salt tea usually starts in childhood and continues for life.12,13 Therefore, salt tea drinking could potentially be an important risk factor and may account for a substantial number of cases of ESCC in this region. To prepare salt tea, people in Kashmir brew green tea leaves, mostly in the presence of baking soda (sodium bicarbonate, NaHCO3), until a thick red-brown colored extract is obtained. During this process, and after partial evaporation of water, more water is added. Based on their personal preference, people dilute the final extract with water and add salt and milk at the end. The tea is repeatedly boiled in a vessel or in a charcoal fueled “samovar,” a vessel commonly used for the beverage preparation in Kashmir, before it is served.

Epidemiology

Salt tea is the most commonly used beverage in Kashmir, India, where esophageal squamous cell carcinoma (ESCC) is the most common cancer. Salt tea is brewed in a unique way in Kashmir, usually with addition of sodium bicarbonate, which makes salt tea alkaline. As little information about the association between salt tea drinking and ESCC was available, we conducted a large-scale case-control study to investigate this association in Kashmir. We recruited 703 histologically confirmed cases of ESCC and 1664 controls individually matched to cases for age, sex, and district of residence. Conditional logistic regression models were used to calculate odds ratios (ORs) and 95% confidence intervals (95% CIs). Participants who consumed >1,250 ml day21 showed an increased risk of ESCC (OR 5 2.60, 95% CIs 5 1.68–4.02). Samovar (a special vessel for the beverage preparation) users (OR 5 1.77, 95% CIs 1.25–2.50) and those who ate cereal paste with salt tea (OR 5 2.14, 95% CIs 5 1.55–2.94) or added bicarbonate sodium to salt tea (OR 5 2.12, 95% CIs 5 1.33–3.39) were at higher risk of ESCC than others. When analysis was limited to alkaline tea drinkers only, those who both consumed cereal paste with salt tea and used samovar vessel were at the highest risk (OR 5 4.58, 95% CIs 5 2.04–10.28). This study shows significant associations of salt tea drinking and some related habits with ESCC risk.

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Salt tea consumption and esophageal cancer

What’s new? Esophageal squamous cell carcinoma (ESCC) is the most common cancer in Kashmir, India. Here the authors report that consumption of salt tea (locally known as Noon Chai), an alkaline green tea prepared with salt, substantially increases risk of ESCC. People who prepared the tea in samovars, added baking soda or poured it over a cereal paste were at highest risk. Although the etiological role of alkaline salt tea in ESCC carcinogenesis remains unclear, these results may help develop preventative strategies to reduce incidence of ESCC in Kashmir and other countries.

Usually, people in Kashmir eat either roti (homemade chapatti or tandoori roti from bakers) or cereal paste (locally called sattu) when they drink salt tea. Tandoori roti is cooked in tandoor, a clay oven heated with charcoal or wood fire. The roasted cereals (mostly rice and maize) are ground to make cereal paste. The paste is placed in a cup and boiling hot tea is poured over it. Salt tea is usually served with breakfast and as afternoon tea.13,14 A case-control study of 200 cases and 200 controls in an adjacent area, Jammu, reported an association between adding baking soda to salt tea and ESCC, but the proportions of cases and controls that drank salt tea were similar.15 However, that study reported no data on dose-response for the observed association. We aimed to investigate in more detail the association between salt tea drinking and ESCC risk in a study of over 700 ESCC cases and 1,600 controls. We report results for the overall association and by amount of use, tea temperature, adding baking soda, and eating cereal paste with and vessels used for preparation of salt tea, with adjustments for several potential confounding factors.

Material and Methods

Epidemiology

Case and control selection

Details of the study design and methods are described elsewhere.9,11,16 Briefly, all histopathologically confirmed ESCC cases were recruited in the Oncology Department of Sher-iKashmir Institute of Medical Sciences (SKIMS), Srinagar, from October 2008 to January 2012. All cases aged 18 years or older and had no previous cancer. For each case, we recruited at least one hospital based control individually matched to the case for sex, age (65 years) and district of residence from in-patient wards of the SKIMS, the Government Medical College Hospital Srinagar and district hospitals. Only patients were enrolled as controls when the disease for which they had been admitted did not have a strong association with tobacco or alcohol consumption. Reasons for hospitalization of controls are provided in Supporting Information Table 1. The controls were recruited within 6 months after their respective cases were recruited. The participation rate was 96% (732 invited, 29 refusals) for cases and 98% (1,697 invited, 33 refusals) for controls. The majority of those who refused were too ill to participate in the study. Informed consent was obtained from all subjects. This study was reviewed and approved by the Institutional Ethics Committee of SKIMS.

Data collection

Face-to-face interviews, using structured questionnaires, were conducted at the hospitals in which study participants were recruited. To minimize inter-individual variation, a limited number of trained researchers conducted the interviews and no proxies were used. Data on socio-demographic factors, including age, sex, ethnicity, religion, place of residence and education were collected. Lifelong history of use of alcohol and several tobacco products, usual intake amount of fresh fruits and vegetables and details on indicators of economic status, including ownership of several appliances, were obtained. Ever use of alcohol and tobacco products was defined as the use of the respective product at least weekly for a period of 6 months or longer. Information on consumption of fruits and vegetables was collected using a semi-quantitative food frequency questionnaire. We asked about the usual frequency of use in a day, week or month and the amount of use in each instance. Using this information, we calculated the intake of each fruit and vegetable in grams per day. To cover the intake of seasonal fruits/vegetables, we also collected data on the number of months in which any of these food items had been consumed: the daily intake in these cases was multiplied by the number of months of consumption and divided by 12. The daily intake of all fruits and vegetables were summed up to estimate the total fruit/vegetable intake per day. We also collected data on tea drinking, including usual quantity consumed per day, drinking temperature, addition of sodium bicarbonate, salt, or milk as ingredients, the use of samovar or other vessels to prepare, boil, or serve salt tea and consumption of roti or cereal paste (sattu) with salt tea. To eliminate any effects of changes in dietary habits in cancer patients, information on diet and salt tea consumption in cases was obtained for 1 year before ESCC being diagnosed. Based on the type of vessels used to prepare and serve salt tea, individuals were grouped into “samovar” users and “other vessels/flask” users. The “other vessel” group prepared salt tea in vessels other than samovar and served the tea directly or after pouring into a vacuum flask. The samovar group prepared, boiled and served salt tea with a samovar. The subjects who use handmade roti (chapatti) or tandoorbaked roti were grouped together and the eaters of different cereal paste were clustered together as cereal paste users. Statistical analysis

Numbers and percentages were calculated and presented for categorical variables. We built a composite score for wealth, C 2014 UICC Int. J. Cancer: 00, 00–00 (2014) V

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Results A total of 703 ESCC cases and 1,664 individually matched controls were recruited in this study. Distribution of demographic factors, wealth score, tobacco and alcohol use, and tea consumption by case status are shown in Table 1. The mean age of cases and controls was 61.6 and 59.8 years, respectively. Approximately 55% of cases and controls were males. The majority of participants (97%) were of Kashmiri ethnic group. About 96% of the subjects were from rural areas. Fresh fruit and vegetable intake among controls was higher than in cases, but hookah, bidi, nass, and gutka use was more frequent in cases. More controls than cases had a higher income. The majority of cases (98.7%) and controls (96.9%) consumed salt tea. Compared to drinking 500 ml salt tea per day, drinking more tea up to 1,250 ml a day was not associated with ESCC risk (Table 2), but drinking > 1,250 ml a day was associated with the risk (OR 5 2.60; 95% CI 5 1.68–4.02). Adding milk to salt tea showed a borderline positive association with ESCC risk in the fully adjusted model. As compared to using other vessels, using samovar to prepare and serve salt tea showed an increased risk of ESCC (OR 5 1.77; 95% CI 5 1.25–2.50). Also, compared to eating roti with salt tea, eating cereal paste was associated with ESCC risk (OR 5 2.14; 95% CI 5 1.55–2.94).

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Table 1. Characteristics of 703 ESCC cases and 1664 controls from Kashmir Valley, India, 2008–20121 Characteristics

Cases (%)

Age, mean (SD), years 61.6 (11.1)

Controls (%) 59.8 (11.1)

Sex

p value

Salt tea consumption and esophageal cancer: a possible role of alkaline beverages in esophageal carcinogenesis.

Salt tea is the most commonly used beverage in Kashmir, India, where esophageal squamous cell carcinoma (ESCC) is the most common cancer. Salt tea is ...
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