A Case–Control Study on Seaweed Consumption and the Risk of Breast Cancer

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A case–control study on seaweed consumption and the risk of breast cancer

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  A case–control study on seaweed consumption and the risk of breast cancer Yoon Jung Yang 1 , Seok-Jin Nam 2 , Gu Kong 3 and Mi Kyung Kim 1 * 1  Department of Preventive Medicine, College of Medicine, Hanyang University, Medical School Building A-Room 512,17 Haengdang Dong, Sungdong Gu, Seoul 133-791, South Korea 2  Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul 135-710,South Korea 3  Department of Pathology, College of Medicine, Hanyang University, Seoul 133-791, South Korea (Received 17 April 2009 – Revised 2 November 2009 – Accepted 4 November 2009 – First published online 8 December 2009) Gim ( Porphyra  sp.) and miyeok ( Undaria pinnatifida ) are the seaweeds most consumed by Koreans. We investigated the association between theintake of gim and miyeok and the risk of breast cancer in a case–control study. Cases were 362 women aged 30–65 years old, who werehistologically confirmed to have breast cancer. Controls visiting the same hospital were matched to cases according to their age ( SD  2 years)and menopausal status. Food intake was estimated by the quantitative FFQ with 121 items, including gim and miyeok. Conditional logisticregression analysis was used to obtain the OR and corresponding 95% CI. The average intake and consumption frequency of gim in caseswere lower than in controls. The daily intake of gim was inversely associated with the risk of breast cancer (5th  v.  1st quintile, OR, 0·48;95% CI, 0·27, 0·86;  P  for trend, 0·026) after adjustment for potential confounders. After stratification analysis was performed according tomenopausal status, premenopausal women (5th  v.  1st quintile, OR, 0·44; 95% CI, 0·24, 0·80;  P  for trend, 0·007) and postmenopausal women(5th  v.  1st quintile, OR, 0·32; 95% CI, 0·13, 0·80;  P  for trend, 0·06) showed similar inverse associations between gim intake and the risk of breast cancer after an adjustment for potential confounders except dietary factors. Miyeok consumption did not have any significant associationswith breast cancer. These results suggest that high intake of gim may decrease the risk of breast cancer. Seaweed: Gim: Miyeok: Breast cancer: Case–control studies Seaweeds have been featured in the diets of Asian culturesince ancient times (1) . The nutritional and physiologicaleffects of seaweeds have received much attention during thepast decades. Seaweeds are rich in polysaccharides, minerals,vitamins and dietary fibre (2–5) . Antioxidant and antimutageniceffects of dietary seaweeds have been reported  in vitro (6–8) and  in vivo  studies (9–11) . Polysaccharides (6,9,12,13) , proteins (14) ,antioxidants (e.g. ascorbate, glutathione and carotenoids) (15,16) ,polyphenols (7) and extracts (7,17) of seaweeds have beenreported to have antioxidant, antitumour and chemoprotectiveactivities.In particular, the potential benefits of seaweed consumptionfor breast cancer treatment have been traced back to theancient Egyptian ‘Ebers Papyrus’, which mentioned thatseaweed was used to treat breast cancer (18) . The putativeprotective effect of seaweed on breast cancer is in accordwith the relatively low breast cancer rates in Japan (19) ,where seaweed-rich diets are consumed and with the increas-ing breast cancer rates in Japanese women who emigrate (20) orconsume a Western style diet (21) . Animal studies (10,22,23) and in vitro  studies (23–25) demonstrated the anticarcinogeniceffects of seaweeds against mammary carcinogenesis. Iodineas well as other components of seaweeds have been suggestedto act as antioxidants (26) and induce apoptosis in human breastcancer cell lines (23) . In an ecological study, the regions whereiodine intake was low had higher breast cancer mortalityrates (27) . However, few epidemiological studies have reportedon the effects of seaweed consumption on breast cancer.Breast cancer is the most common cancer in Koreanwomen, with an age-standardised incidence rate of 31·1 per100000 persons in 2002 (28) . Even though the incidence rateof breast cancer is lower than in Western countries (19) , thisrate has been increasing in Korea (29) . Seaweed is frequentlyconsumed on a daily basis in a traditional Korean diet.According to the third Korean National Health and NutritionSurvey (2005) (30) , the daily intake of seaweed was 8·5g/d(fresh  þ  dry mass). Gim ( Porphyra  sp.), miyeok ( Undaria pinnatifida ; ‘wakame’ in Japan) and dashima (  Laminaria  sp.;‘konbu’ in Japan) are common seaweeds, which constituteover 95% of seaweed consumption in Korea (30) . However,dashima (  Laminaria  sp.) is usually used for making broth(i.e. soaked in boiling water then removed), so that theactual intake is not substantial. Gim is a Korean style edibleseaweed in the genus  Porphyra . Gim ( Porphyra  sp.) lookslike ‘nori’ in Japan, but sheets of gim are thinner than norisheets. Seasoned roasted gim prepared with sesame oil andsalts is the most common type of gim and it is consumed asa side dish. Gim is also used as wrappings, seasonings and * Corresponding author:  Mi Kyung Kim, fax  þ 82 2 2293 0660, email kmkkim@hanyang.ac.kr  British Journal of Nutrition  (2010),  103 , 1345–1353 doi:10.1017/S0007114509993242 q  The Authors 2009      B   r     i    t     i   s     h     J   o   u   r   n   a     l   o     f     N   u    t   r     i    t     i   o   n  condiments. Miyeok ( U. pinnatifida ) is the second mostcommonly consumed seaweed in Korea and is usuallyconsumed as the form of soup or a side dish.Despite high consumption of seaweeds in Asian countries,the association between seaweed consumption and breastcancer risk has been determined in limited epidemiologicalstudies (31) . Thus, the aim of the present study was to investi-gate the association between the consumption of seaweed,specifically gim ( Porphyra  sp.) and miyeok ( U. pinnatifida ),and the risk of breast cancer in a case–control study amongKorean women. Material and methods Cases and controls Cases and controls were recruited from October 2004 to June2006 at Samsung Hospital of Sungkyunkwan University inSeoul, South Korea. All participants aged 30–65 years wereexamined by mammography to detect any possibility of breast cancer. Cases had histologically confirmed breastcancer. Subjects having any history of cancer (five cases) orhaving an estimated total energy intake , 2092kJ/d( , 500kcal/d) or . 16736kJ/d ( . 4000kcal/d; sixteen casesand thirteen controls) were excluded from the study. Controlswere patients visiting one of the dentistry, orthopedic surgery,general surgery, ophthalmology, dermatology, rehabilitation,obstetrics and gynecology or family medicine clinics withinthe same hospital. Cases and controls were matched bytheir age (within 2 years) and menopausal status (362 pairs).The present study was conducted according to the guidelineslaid down in the Declaration of Helsinki and all proce-dures involving the human subjects were approved by theInstitutional Review Board of the Samsung Hospital of Sungkyunkwan University. Written informed consent wasobtained from all the subjects.  Data collection Cases and controls were interviewed by trained interviewerswith a questionnaire addressing patients’ general character-istics, menstrual and reproductive history, family history of breast cancer, smoking and drinking habits, intake of multi-vitamins and the average time spent on exercising. Dietarydata were collected by the quantitative FFQ, which weremodified from the validated FFQ (32) , with visual aids suchas food photographs and models for item-specific units. TheFFQ was composed of 121 food items which included roastedgim ( Porphyra  sp.) and miyeok soup ( U. pinnatifida ). The gimused as wrappings, seasonings and condiments was not askedin the questionnaire. The amounts of foods consumed wereasked in open-ended questions with standard units such ascup, bowl and piece etc. Subjects were asked by trainedinterviewers to recall their usual intake of the 121 fooditems over a period of 12 months beginning from 3 yearsbefore the time of the interview (33) . All frequencies werestandardised into ‘times/day’ by using the conversion factors4·3 weeks/month and 30·4d/month. Daily food intake was cal-culated with standardised frequency per day and the amountof food consumed. Detailed information on data collectionhas been presented in previous publications elsewhere (34,35) .The intake of gim and miyeok was calculated using standar-dised frequency per day and one portion per unit. One sheet of dried, roasted gim was 2g in dry mass and one portion of miyeok soup was composed of 36g of miyeok in freshmass. Nutrient intakes adjusted for total energy intake bythe residual method were used in all the analyses to avoidbias due to the simple relationship of nutrient intake withtotal energy intake. Statistical analysis All statistical analyses were performed using the SAS software(version 9.1; SAS Institute, Inc., Cary, NC, USA). Cases andtheir matched controls were compared by a paired  t   test forcontinuous variables and by the McNemar test for categoricalvariables. The quintiles of daily gim intake, consumptionfrequency of gim and daily miyeok intake were applied tothe analyses. Since the variation of miyeok consumptionfrequency was not large, it could not be classified into quintilegroups, thus, the quartiles of miyeok consumption frequencywere applied to the analyses. In addition, the menopausalstatus-specific quintiles were used in the subgroup analysisof menopausal status. The general linear model and theCochran–Mantel–Haenzel analysis were used to determinepotential confounders among the controls. Conditional logisticregression analysis was applied to obtain the OR and corres-ponding 95% CI. Three different models were applied toexamine the associations of seaweed intake with the risk of breast cancer. Any variable was not adjusted in the firstmodel. Variables which were significantly different betweenthe cases and controls and showed significant linear trendsacross quintiles or quartiles of seaweed intake except dietaryvariables were adjusted in the second model. Dietary variableswere additionally adjusted in the third model. The trend testswere conducted by treating the median values of each quintileas continuous variables in a multivariate model after inputtingthe median value of the controls into each dietary intakegroup. Daily intakes of gim and miyeok and the averageconsumption frequencies of gim and miyeok were also intro-duced as continuous variables, and the units were expressedin increments of 1g/d and once per week, respectively. Results The characteristics of the breast cancer cases and thematched controls are presented in Table 1. Compared with thecontrols, the cases had lower proportions of multivitaminusers and breast feeding and had fewer children. The casesconsumed lower amounts of soya protein, mushrooms and gim( Porphyra  sp.) than the controls. The frequency of gimintakewasalsolowerinthecasesthaninthecontrols.However,the intake of miyeok and the average consumption frequencyof miyeok did not differ between the cases and the controls.To determine any potential confounding factors, the distri-butions of selected characteristics of the control subjectswere examined by using the quintiles of gim intake, frequencyof gim intake and miyeok intake, as well as the quartiles of frequency of miyeok intake (Table 2). Education, physicalactivity and oral contraceptive use increased across thequintiles of gim intake in the controls. The proportion witha family history of breast cancer decreased across the quintiles Y. J. Yang  et al. 1346      B   r     i    t     i   s     h     J   o   u   r   n   a     l   o     f     N   u    t   r     i    t     i   o   n  of the frequency of gim intake, miyeok intake and thefrequency of miyeok intake. The proportion of exerciseincreased across the quintiles of the gim intake frequency.The intakes of energy,  b -carotene, vitamin C, folate andvitamin E increased across the quintiles of gim intake, thefrequency of gim intake, miyeok intake and the frequency of miyeok intake. The intake of soya protein increased acrossthe quintiles of gim intake and the frequency of gim intake.The variables showing significant trends according to theconsumptions of gim and miyeok in Table 2 are adjusted aspotential confounding factors in Tables 3 and 4.The associations between seaweed and the risk of breastcancer are given in Table 3. A significant inverse associationwas found between the breast cancer risk and gim intake(OR, 0·47; 95% CI, 0·29, 0·75 for the last quintile in compari-son with the lowest quintile;  P  for trend, 0·003). The inverseassociation between breast cancer risk and gim intake wassignificant after adjusting for potential confounders such asmultivitamin supplement, number of children, breast feeding,education, exercise and oral contraceptive use (OR, 0·43;95% CI, 0·26, 0·70 for the last quintile;  P  for trend, 0·002).After an additional adjustment for the dietary potentialconfounders (quintiles of energy as well as consumption of  b -carotene, vitamin C, folate, vitamin E, soya protein andmushrooms), the inverse association between breast cancerrisk and gim intake remained (OR, 0·48; 95% CI, 0·27, 0·86for the last quintile;  P  for trend, 0·026). In the analyses withcontinuous data, gim intake showed inverse associationswith breast cancer risk in the three models. A consumptionfrequency of gim was also inversely associated with breastcancer risk (OR, 0·52; 95% CI, 0·32, 0·84 for the last quintile; P  for trend ¼ 0·009). The inverse association of the consump-tion frequency of gim with the breast cancer risk remainedafter adjusting for potential confounders including a multi-vitamin supplement use, number of children, breast feeding,a family history of breast cancer and exercise (OR, 0·51;95% CI, 0·30, 0·84 for the last quintile;  P  for trend, 0·018).However, after the additional adjustment for dietary poten-tial confounders (quintiles of energy as well as intake of  b -carotene, vitamin C, folate, vitamin E, soya protein andmushrooms), the inverse association between breast cancerrisk and consumption frequency of gim was no longer signifi-cant (OR, 0·58; 95% CI, 0·32, 1·04 for the last quintile;  P  fortrend, 0·144). In the analyses with the continuous data, thesignificant inverse associations between breast cancer risk and the consumption frequency of gim were found in thecrude OR (OR, 0·93; 95% CI, 0·88, 0·98) and in the multi-variate model 1 (OR, 0·93; 95% CI, 0·88, 0·98). Miyeok intake and the frequency of miyeok intake did not show anysignificant associations with the risk of breast cancer. Table 1.  General characteristics of the study subjects with or without breast cancer(Mean values and standard deviations or proportions)Case ( n   362) Control ( n   362)Characteristics Mean  SD  Mean  SD  P  *Age (years) 46·1 8·5 46·0 8·6 NAEducation (years) 12·7 3·6 12·4 3·5 0·307BMI (kg/m 2 ) 23·6 3·2 23·4 3·0 0·410Alcohol intake (g/d) 1·9 6·2 2·4 8·1 0·295Number of children 1·9 1·0 2·1 1·0 0·010Age at menarche (years) 14·5 1·7 14·5 1·7 0·407Age at first birth (years) 26·0 3·5 25·8 3·4 0·836Age at menopause (years) 48·0 5·4 48·4 5·2 0·110Dietary intakeEnergy (kJ/d) 8136·2 2389·1 8474·7 2753·9 0·305 b -Carotene† ( m g/d) 4381·1 7289·5 4160·3 2367·6 0·584Vitamin C† (mg/d) 151·7 91·7 146·9 79·1 0·440Folate† ( m g/d) 283·8 100·4 296·9 99·9 0·067Vitamin E† (mg/d) 10·6 4·1 11·2 4·3 0·088Fiber† (g/d) 10·1 4·5 10·1 4·1 0·964Soya protein (g/d) 7·4 4·5 8·5 4·6 0·001Mushroom (g/d) 7·8 10·0 11·4 21·2 0·005Gim (g: dry mass/d) 0·86 0·93 1·17 1·43  , 0·001Gim (frequency/week) 3·01 2·85 3·76 3·72 0·002Miyeok (g: fresh mass/d) 5·12 5·57 5·45 5·80 0·426Miyeok (frequency/week) 1·10 1·10 1·15 1·13 0·499Menopausal women (%) 35 35 NAFamily history of breast cancer (%) 8 12 0·099Current smoker (%) 2 4 0·127Regular exercise ( $ 22·5MET-h/week) (%) 17 22 0·110Multivitamin user (%) 9 14 0·030Parity (%) 89 92 0·131Oral contraceptive use (ever) (%) 15 14 0·831Breast feeding (ever) (%) 64 77  , 0·001Used hormone compound (ever) (%) 14 14 0·821 NA, not applicable; MET, metabolic equivalent.*Two-sided; paired  t   test for continuous variables and McNemar test for categorical variables.†All nutrients were total energy-adjusted by a residual method after log transformation. Seaweed consumption and breast cancer 1347      B   r     i    t     i   s     h     J   o   u   r   n   a     l   o     f     N   u    t   r     i    t     i   o   n
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