This article was downloaded by: [New York University] On: 31 July 2015, At: 07:53 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: 5 Howick Place, London, SW1P 1WG
Nutrition and Cancer Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/hnuc20
Dietary Intake and Serum Level of Carotenoids in Lung Cancer Patients: A Case-Control Study a
a
b
Somayeh Asbaghi , Ahmad Saedisomeolia , Mostafa Hosseini , Niyaz Mohammadzadeh a
c
Honarvar , Adnan Khosravi & Eznollah Azargashb
d
a
Department of Cellular and Molecular Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran b
Department of Epidemiology and Biostatistics, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran c
Masih-Daneshvari Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran
d
Click for updates
School of Public Health, Shahid Beheshti University of Medical Sciences, Tehran, Iran Published online: 13 Jul 2015.
To cite this article: Somayeh Asbaghi, Ahmad Saedisomeolia, Mostafa Hosseini, Niyaz Mohammadzadeh Honarvar, Adnan Khosravi & Eznollah Azargashb (2015): Dietary Intake and Serum Level of Carotenoids in Lung Cancer Patients: A Case-Control Study, Nutrition and Cancer, DOI: 10.1080/01635581.2015.1055365 To link to this article: http://dx.doi.org/10.1080/01635581.2015.1055365
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Nutrition and Cancer, 0(0), 1–6 Copyright Ó 2015, Taylor & Francis Group, LLC ISSN: 0163-5581 print / 1532-7914 online DOI: 10.1080/01635581.2015.1055365
Dietary Intake and Serum Level of Carotenoids in Lung Cancer Patients: A Case-Control Study Somayeh Asbaghi and Ahmad Saedisomeolia Department of Cellular and Molecular Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran
Mostafa Hosseini Department of Epidemiology and Biostatistics, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
Downloaded by [New York University] at 07:53 31 July 2015
Niyaz Mohammadzadeh Honarvar Department of Cellular and Molecular Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran
Adnan Khosravi Masih-Daneshvari Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran
Eznollah Azargashb School of Public Health, Shahid Beheshti University of Medical Sciences, Tehran, Iran
The aim of this study was to compare the dietary intake and serum levels of some selected carotenoids of lung cancer patients with healthy subjects. Thirty-five lung cancer patients and 33 healthy people were enrolled into this case-control study. Daily intake of nutrients was estimated using a semiquantitative food frequency questionnaire and a 3-day 24-h food recall questionnaire. The concentration of serum beta-carotene and lycopene were analyzed using a high performance liquid chromatography method. Case and control groups did not differ by the means of age, gender, smoking habits, weight, body mass index, mean daily energy intake, mean daily fat intake, and the percentage of daily energy provided by fat to total daily energy intake. The beta-carotene and lycopene intake of the case subjects was 96% and 195% greater than that of the control subjects. Daily intake of fruits and vegetables in the cancer group was higher than the control group. However, the serum concentration of 118% beta-carotene and 60% lycopene were higher in the control group. Despite a higher daily dietary intake of betacarotene and lycopene by lung cancer patients, serum betacarotene and lycopene concentrations were significantly lower than the group without cancer.
Submitted 30 March 2014; accepted in final form 20 May 2015. Address correspondence to Ahmad Saedisomeolia, Department of Cellular and Molecular Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran. Phone: 0098 21 88955742 (office). E-mail: [email protected]
INTRODUCTION Respiratory disease such as lung cancer is one of the most prevalent diseases in the world and it is expected to be the main cause of death by 2020 (1). Lung cancer is a disease of malignant lung cells that usually occurs in the cells lining the airways (2). Carcinoma of the lung is one of the most prevalent human solid cancers. In 2008, it accounted for around 12.7% of all new cancer incidence and 18.2% of all cancer mortality, or approximately 1.4 million deaths worldwide (2,3), and the fifth leading malignancy in Iran (4). The incident of lung cancer is increasing among men and women (4,5). Despite the great progress in the treatment of the lung cancer, a 5-yr survival rate after diagnosis is reportedly around 14% in the United States (4) and 10.15% in Iran (5). Free radicals are molecules causing oxidative stress in cells by disrupting the balance between oxidation and reduction (6,7). This situation leads to the progression of many diseases, including Alzheimer’s, rheumatoid arthritis, atherosclerosis, and different types of cancers (8,9). Smoking is the main cause of lung cancer by inducing oxidative stress to the lung cells (9). Epidemiological studies in different populations have shown that the incidence of lung cancer is inversely associated with the consumption of fruits and vegetables (3,10,11). Antioxidants are substances preventing oxidation of vital molecules in the body via the elimination of free radicals (12). 1
Downloaded by [New York University] at 07:53 31 July 2015
2
S. ASBAGHI ET AL.
Carotenoids are fat-soluble pigments found in plants (13). The orange color of carrots, citrus fruits, and red color of tomatoes and peppers is due to their carotenoid content (14). About 600 types of carotenoids have been identified in nature (14). Evidence from observational and prospective studies demonstrated protective effects of fruits and vegetables on lung cancer risk (15). The protective effect of antioxidant-rich carotenoids may explain this inverse association (16). Several recent studies have found some new anticarcinogenic mechanisms by which carotenoids induce the inhibition of the activity of nuclear factor kappa B (NFkB), and also exert antiprolifrative and apoptotic activities (17–19). Human body cannot synthesize carotenoids; therefore, it depends on the dietary or supplementary intake (20). About 40 types of carotenoids are found in human food and 21 types in the human serum (21). The most common carotenoids in human serum include lycopene, alpha-carotene, beta-carotene, b-cryptoxanthin, and lutein (22). Lycopene has the most potential antioxidant effect among carotenoids (23,24), and beta-carotene is the most abundant carotenoid in the human body (25). Therefore, it is expected these 2 carotenoids play a key beneficial role in reducing the risk of lung cancer (17). The vast majority of current evidence on associations of dietary pattern with lung cancer is derived from populations in North America and Europe. The role of dietary intake on lung cancer in Iran has not been well investigated yet (19). This study is aimed to determine the serum level of lycopene and beta-carotene, as well as their dietary intake in people with and without lung cancer as a case-control study.
EXPERIMENTAL METHODS Study Population This case-control study was conducted in 2012 on lung cancer patients as a research project in Tehran University of Medical Sciences (TUMS). In this study, the patients referred to The Oncology Department of Firoozgar, Shariati, and Masih Daneshvari Hospitals (Tehran, Iran) were enrolled into the study. Patients diagnosed with lung cancer of Stages 2 and 3 from pathological standpoint, were considered as a “case” and subjects without lung cancer as a “control.” Thirty-five cancer patients and 33 healthy subjects were enrolled into the study. At the beginning of the study, a written informed consent form (approved by the Ethics Committee of TUMS, reference no: 90-04-27-16334), was obtained from all participants. The exclusion criteria for the case group were suffering from Stage 4 of lung cancer, existence of any kind of metastasis, initiation of chemo- and radiotherapy, use of any kind of antioxidant or carotenoids supplements, consumption of alcohol, suffering from inflammatory disease or diabetes, and hormone replacement therapy in menopause women. The control group was recruited by public announcements from the Tehran resident population via posters around the hospitals neighborhood. In
the control group, 33 volunteers without lung cancer were matched with case group by the means of age, gender, and smoking habits.
Anthropometric Assessments Height was measured without shoes as subjects drew a deep breath and were asked to stand tall. The weight (with an accuracy of 0.1 kg) was measured using a scale (Seca Hamburg, Germany) with minimal light clothing.
Dietary Assessment To estimate daily dietary intake of carotenoids (beta-carotene and lycopene) during the past year, a semiquantitative food frequency questionnaire including 33 food items (11 fruits and 21 vegetables) was used. Values were converted to mg/day by using National Nutrition Database for U.S. Department of Agriculture and Nationwide Food Consumption Survey. To estimate daily intake of energy, macronutrients, and micronutrients, a 24-h dietary recall questionnaire (for 3 days including 2 weekdays and a weekend) was used. Subjects were assisted to remember all consumed meals and food items, as well as their amounts. Both forms were previously validated for Iranian foods (26). Nutritionist 4 Software (San Bruno, CA) was used to estimate daily dietary intake amounts.
Blood Sampling and Carotenoid Analysis Five ml nonfasting blood samples were taken from all subjects. The subjects were asked to stay at the clinic 10 min after blood sampling, to avoid any possible complications due to collection of samples. The serum was separated from whole blood and frozen at ¡80 C until they were used in the laboratory. Lycopene and beta-carotene were extracted from the serum and measured using HPLC, Yong Lin, Nova-Pak C18 column (Waters, Milford, MA), isocratic pump, and UV detector according the method we previously developed (27).
Statistical Analysis The Statistical Package for Social Sciences (version 16 for Windows) was used to compare variables between the case and control groups. Data are expressed as mean § SD. Departure from normality was assessed using the Kolmogorov–Smirnov distribution test. For qualitative variables the chi-square test and for quantitative variables independent t-test were used. Significance level was considered as
Nutrition and Cancer Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/hnuc20
Dietary Intake and Serum Level of Carotenoids in Lung Cancer Patients: A Case-Control Study a
a
b
Somayeh Asbaghi , Ahmad Saedisomeolia , Mostafa Hosseini , Niyaz Mohammadzadeh a
c
Honarvar , Adnan Khosravi & Eznollah Azargashb
d
a
Department of Cellular and Molecular Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran b
Department of Epidemiology and Biostatistics, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran c
Masih-Daneshvari Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran
d
Click for updates
School of Public Health, Shahid Beheshti University of Medical Sciences, Tehran, Iran Published online: 13 Jul 2015.
To cite this article: Somayeh Asbaghi, Ahmad Saedisomeolia, Mostafa Hosseini, Niyaz Mohammadzadeh Honarvar, Adnan Khosravi & Eznollah Azargashb (2015): Dietary Intake and Serum Level of Carotenoids in Lung Cancer Patients: A Case-Control Study, Nutrition and Cancer, DOI: 10.1080/01635581.2015.1055365 To link to this article: http://dx.doi.org/10.1080/01635581.2015.1055365
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Nutrition and Cancer, 0(0), 1–6 Copyright Ó 2015, Taylor & Francis Group, LLC ISSN: 0163-5581 print / 1532-7914 online DOI: 10.1080/01635581.2015.1055365
Dietary Intake and Serum Level of Carotenoids in Lung Cancer Patients: A Case-Control Study Somayeh Asbaghi and Ahmad Saedisomeolia Department of Cellular and Molecular Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran
Mostafa Hosseini Department of Epidemiology and Biostatistics, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
Downloaded by [New York University] at 07:53 31 July 2015
Niyaz Mohammadzadeh Honarvar Department of Cellular and Molecular Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran
Adnan Khosravi Masih-Daneshvari Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran
Eznollah Azargashb School of Public Health, Shahid Beheshti University of Medical Sciences, Tehran, Iran
The aim of this study was to compare the dietary intake and serum levels of some selected carotenoids of lung cancer patients with healthy subjects. Thirty-five lung cancer patients and 33 healthy people were enrolled into this case-control study. Daily intake of nutrients was estimated using a semiquantitative food frequency questionnaire and a 3-day 24-h food recall questionnaire. The concentration of serum beta-carotene and lycopene were analyzed using a high performance liquid chromatography method. Case and control groups did not differ by the means of age, gender, smoking habits, weight, body mass index, mean daily energy intake, mean daily fat intake, and the percentage of daily energy provided by fat to total daily energy intake. The beta-carotene and lycopene intake of the case subjects was 96% and 195% greater than that of the control subjects. Daily intake of fruits and vegetables in the cancer group was higher than the control group. However, the serum concentration of 118% beta-carotene and 60% lycopene were higher in the control group. Despite a higher daily dietary intake of betacarotene and lycopene by lung cancer patients, serum betacarotene and lycopene concentrations were significantly lower than the group without cancer.
Submitted 30 March 2014; accepted in final form 20 May 2015. Address correspondence to Ahmad Saedisomeolia, Department of Cellular and Molecular Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran. Phone: 0098 21 88955742 (office). E-mail: [email protected]
INTRODUCTION Respiratory disease such as lung cancer is one of the most prevalent diseases in the world and it is expected to be the main cause of death by 2020 (1). Lung cancer is a disease of malignant lung cells that usually occurs in the cells lining the airways (2). Carcinoma of the lung is one of the most prevalent human solid cancers. In 2008, it accounted for around 12.7% of all new cancer incidence and 18.2% of all cancer mortality, or approximately 1.4 million deaths worldwide (2,3), and the fifth leading malignancy in Iran (4). The incident of lung cancer is increasing among men and women (4,5). Despite the great progress in the treatment of the lung cancer, a 5-yr survival rate after diagnosis is reportedly around 14% in the United States (4) and 10.15% in Iran (5). Free radicals are molecules causing oxidative stress in cells by disrupting the balance between oxidation and reduction (6,7). This situation leads to the progression of many diseases, including Alzheimer’s, rheumatoid arthritis, atherosclerosis, and different types of cancers (8,9). Smoking is the main cause of lung cancer by inducing oxidative stress to the lung cells (9). Epidemiological studies in different populations have shown that the incidence of lung cancer is inversely associated with the consumption of fruits and vegetables (3,10,11). Antioxidants are substances preventing oxidation of vital molecules in the body via the elimination of free radicals (12). 1
Downloaded by [New York University] at 07:53 31 July 2015
2
S. ASBAGHI ET AL.
Carotenoids are fat-soluble pigments found in plants (13). The orange color of carrots, citrus fruits, and red color of tomatoes and peppers is due to their carotenoid content (14). About 600 types of carotenoids have been identified in nature (14). Evidence from observational and prospective studies demonstrated protective effects of fruits and vegetables on lung cancer risk (15). The protective effect of antioxidant-rich carotenoids may explain this inverse association (16). Several recent studies have found some new anticarcinogenic mechanisms by which carotenoids induce the inhibition of the activity of nuclear factor kappa B (NFkB), and also exert antiprolifrative and apoptotic activities (17–19). Human body cannot synthesize carotenoids; therefore, it depends on the dietary or supplementary intake (20). About 40 types of carotenoids are found in human food and 21 types in the human serum (21). The most common carotenoids in human serum include lycopene, alpha-carotene, beta-carotene, b-cryptoxanthin, and lutein (22). Lycopene has the most potential antioxidant effect among carotenoids (23,24), and beta-carotene is the most abundant carotenoid in the human body (25). Therefore, it is expected these 2 carotenoids play a key beneficial role in reducing the risk of lung cancer (17). The vast majority of current evidence on associations of dietary pattern with lung cancer is derived from populations in North America and Europe. The role of dietary intake on lung cancer in Iran has not been well investigated yet (19). This study is aimed to determine the serum level of lycopene and beta-carotene, as well as their dietary intake in people with and without lung cancer as a case-control study.
EXPERIMENTAL METHODS Study Population This case-control study was conducted in 2012 on lung cancer patients as a research project in Tehran University of Medical Sciences (TUMS). In this study, the patients referred to The Oncology Department of Firoozgar, Shariati, and Masih Daneshvari Hospitals (Tehran, Iran) were enrolled into the study. Patients diagnosed with lung cancer of Stages 2 and 3 from pathological standpoint, were considered as a “case” and subjects without lung cancer as a “control.” Thirty-five cancer patients and 33 healthy subjects were enrolled into the study. At the beginning of the study, a written informed consent form (approved by the Ethics Committee of TUMS, reference no: 90-04-27-16334), was obtained from all participants. The exclusion criteria for the case group were suffering from Stage 4 of lung cancer, existence of any kind of metastasis, initiation of chemo- and radiotherapy, use of any kind of antioxidant or carotenoids supplements, consumption of alcohol, suffering from inflammatory disease or diabetes, and hormone replacement therapy in menopause women. The control group was recruited by public announcements from the Tehran resident population via posters around the hospitals neighborhood. In
the control group, 33 volunteers without lung cancer were matched with case group by the means of age, gender, and smoking habits.
Anthropometric Assessments Height was measured without shoes as subjects drew a deep breath and were asked to stand tall. The weight (with an accuracy of 0.1 kg) was measured using a scale (Seca Hamburg, Germany) with minimal light clothing.
Dietary Assessment To estimate daily dietary intake of carotenoids (beta-carotene and lycopene) during the past year, a semiquantitative food frequency questionnaire including 33 food items (11 fruits and 21 vegetables) was used. Values were converted to mg/day by using National Nutrition Database for U.S. Department of Agriculture and Nationwide Food Consumption Survey. To estimate daily intake of energy, macronutrients, and micronutrients, a 24-h dietary recall questionnaire (for 3 days including 2 weekdays and a weekend) was used. Subjects were assisted to remember all consumed meals and food items, as well as their amounts. Both forms were previously validated for Iranian foods (26). Nutritionist 4 Software (San Bruno, CA) was used to estimate daily dietary intake amounts.
Blood Sampling and Carotenoid Analysis Five ml nonfasting blood samples were taken from all subjects. The subjects were asked to stay at the clinic 10 min after blood sampling, to avoid any possible complications due to collection of samples. The serum was separated from whole blood and frozen at ¡80 C until they were used in the laboratory. Lycopene and beta-carotene were extracted from the serum and measured using HPLC, Yong Lin, Nova-Pak C18 column (Waters, Milford, MA), isocratic pump, and UV detector according the method we previously developed (27).
Statistical Analysis The Statistical Package for Social Sciences (version 16 for Windows) was used to compare variables between the case and control groups. Data are expressed as mean § SD. Departure from normality was assessed using the Kolmogorov–Smirnov distribution test. For qualitative variables the chi-square test and for quantitative variables independent t-test were used. Significance level was considered as
