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Keywords:

  • mushrooms;
  • menopausal status;
  • breast cancer;
  • case–control study

Abstract

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Results
  5. Discussion
  6. Acknowledgements
  7. References

To evaluate the association between dietary mushroom intake and breast cancer risk, a total of 362 women between the ages of 30 and 65 years who were histologically confirmed to have breast cancer were matched to controls by age (±2 years) and menopausal status. Mushroom intake was measured via a food frequency questionnaire that was administered by well-trained interviewers. The associations between the daily intake and the average consumption frequency of mushrooms with breast cancer risk were evaluated using matched data analysis. Both the daily intake (5th vs. 1st quintile, OR = 0.48, 95% CI = 0.30–0.78, p for trend 0.030) and the average consumption frequency of mushrooms (4th vs. 1st quartile, OR = 0.54, 95% CI = 0.35–0.82, p for trend 0.008) were inversely associated with breast cancer risk after adjustment for education, family history of breast cancer, regular exercise [≥22.5 MET (metabolic equivalent)-hr/week], BMI (body mass index, Kg/m2), number of children and whether they are currently smoking, drinking or using multivitamin supplements. Further adjustments were made for energy-adjusted carbohydrate, soy protein, folate and vitamin E levels, which tended to attenuate these results. After a stratification was performed according to menopausal status, a strong inverse association was found in postmenopausal women (OR = 0.16, 95% CI = 0.04–0.54, p for trend = 0.0058 for daily intake; OR = 0.17, 95% CI = 0.05–0.54, p for trend = 0.0037 for average frequency), but not in premenopausal women. In conclusion, the consumption of dietary mushrooms may decrease breast cancer risk in postmenopausal women. © 2007 Wiley-Liss, Inc.

Mushrooms have been consumed worldwide to maintain general human health because of the general understanding that mushrooms are excellent sources of nutrition. A number of bioactive compounds have been identified in many mushroom species.1, 2 The most actively investigated mushroom-derived substances are the polysaccharides, which have antitumor and immunomodulating properties.1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11 The extracts of mushroom have been increasingly sold as dietary supplements based on the claim that they enhance immune fractions and promote health.12 However, there are little data available on the potential preventive benefits of mushrooms as dietary constituents. To our knowledge, there have only been 3 epidemiologic studies13, 14, 15 that have researched the association between mushroom intake and cancer risk (2 on stomach cancer and 1 on breast cancer). All of these studies were performed in Asian countries (2 in Korea13, 15 and 1 in Japan14).

Korea is widely known for its consumption of mushrooms with medicinal properties to promote health and to prevent or treat diseases.2, 16 This is the reason why we previously initiated a study on the effect of mushroom intake on common cancers in Korea and found an inverse association between mushroom intake and stomach cancer,13 which is one of the main causes of death among Koreans. Breast cancer is the second most common cancer following stomach cancer17 in Korean women. Results from a recent case–control study on breast cancer among Korean women suggested the possibility of preventing breast cancer by consuming a diet high in mushrooms.15

The aim of this case–control study is to investigate the association between dietary mushrooms and the risk of breast cancer among Korean women between the ages of 30 and 65 years.

Material and methods

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Results
  5. Discussion
  6. Acknowledgements
  7. References

Cases and controls

Cases and controls were recruited at Samsung Hospital of Sungkyunkwan University in Seoul, South Korea, from October 2004 to June 2006. Participants were between the ages of 30 and 65 years and were all examined with a mammography to confirm the presence of breast cancer. Subjects were excluded from the study if they had any history of cancer (5 cases) and had an estimated total energy intake <500 kcal/day or >4,000 kcal/day (16 cases and 13 controls). Controls were patients who had visited one of the dentistry, orthopedic surgery, general surgery, ophthalmology, dermatology, rehabilitation, obstetrics and gynecology or family medicine clinics within the same hospital. All histologically confirmed cases were matched to controls by their age (within 2 years) and menopausal status (362 pairs). The Institutional Review Board (IRB) of the Samsung Hospital of Sungkyunkwan University approved this study and written informed consent forms were obtained from all study participants.

Data collection

Trained interviewers administered the questionnaires that addressed patients' general characteristics, menstrual and reproductive history, family history of breast cancer, smoking and drinking habits, intake of multivitamins and the average time spent exercising. To collect dietary data, the quantitative food frequency questionnaire (FFQ) was used with visual aids, such as food photographs and models, to demonstrate item-specific units, which was modified from the validated FFQ.18 Subjects were asked by trained dietitians to recall their diet from 3 years prior to the time of the interview by asking them to provide their usual intake of 121 food items over a period of 12 months.19 Portion sizes were open-ended questions and standard units were used for all food items. All frequencies were standardized into “times per day” by using the conversion factors 30.4 days or 4.3 weeks per month. The food intake and nutrient intake per day was calculated using a weighted frequency per day, a portion size per unit and 2 databases with recipe and nutrient information.20 To avoid bias due to the simple relationship between nutrient intake and total energy intake, the nutrient intake results were used only after the residual method was used to adjust for total energy intake.19

Statistical analysis

Statistical analyses were conducted using the SAS (version 9.1) software. Comparisons between cases and their matched controls were conducted by a paired t-test for continuous variables and by the McNemar test for categorical variables. The quintiles of daily intake and the quartiles of the average consumption frequency of mushroom intake were used in the analyses and the menopausal status specific quantiles were used in subgroup analysis by menopausal status. The general linear model and the Cochran Mantel Haenszel analysis were used to assess potential confounders among controls. Conditional logistic regression analysis was used in the multivariate analyses for the matched data. The trend tests were conducted by treating the median values of each quantile of daily mushroom intake or its average consumption frequency as continuous values in each of the models. Daily intake and the average consumption frequency of mushroom were also introduced as continuous variables, and the units were expressed in increments of 15 g/day and once/week, respectively.

Results

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Results
  5. Discussion
  6. Acknowledgements
  7. References

The average age of cases and controls was 46 years, and the proportion of menopausal women was 35%. Women in the control group had more children than the group consisting of cases. Similarly, the proportions of women who were alcohol drinkers and multivitamin users and who had breastfed were consistently higher in the control group than in the cases. Dietary intakes of soy protein (8.53 g/day for controls vs. 7.38 g/day for cases), and mushroom intake (11.4 g/day for controls vs. 7.81 g/day for cases) were also higher in controls, but the carbohydrate intake was higher in cases (312 g/day for controls vs. 320 g/day for cases) (Table I).

Table I. General Characteristics of Study Subjects With and Without Breast Cancer
CharacteristicsCases (n = 362)Controls (n = 362)p value
  1. N/A, not applicable. All nutrient consumptions were adjusted for total energy intake. Values are expressed as Mean ± SD or Number (Percent). p-value: two-sided; paired t-test for continuous variables and McNemar test for categorical variables.

Age (year)46.1 ± 8.4846.0 ± 8.62N/A
Menopausal women (%)127 (35)127 (35)N/A
Education (year)12.7 ± 3.5812.4 ± 3.540.3074
Body mass index (Kg/m2)23.6 ± 3.2123.4 ± 2.980.4097
Family history of breast cancer (%)30 (8.29)44 (12.2)0.0990
Current smoker (%)7 (1.93)14 (3.87)0.1266
Current alcohol drinker (%)104 (28.7)136 (37.6)0.0072
Regular exercise (≥22.5 MET-hr/week, %)61 (16.9)78 (21.6)0.1098
Multivitamin user (%)32 (8.84)51 (14.1)0.0304
Parity (%)323 (89.2)334 (92.3)0.1308
Number of children1.93 ± 1.002.1 ± 0.990.0104
Oral contraceptive use (ever, %)53 (14.6)51 (14.1)0.8312
Breast feeding (ever, %)231 (63.8)277 (76.5)<0.0001
Used hormone compound (ever, %)52 (14.4)50 (13.8)0.8208
Age at menarche (year)14.5 ± 1.6514.5 ± 1.710.4069
Age at first birth (year)26.0 ± 3.4525.8 ± 3.440.8361
Age at menopause (year)48.0 ± 5.4248.4 ± 5.150.1104
Dietary intake   
 Energy (kcal/day)1944 ± 5722026 ± 6580.0728
 Carbohydrate (g/day)320 ± 41.1312 ± 40.70.0077
 Soy protein (g/day)7.38 ± 4.498.53 ± 4.620.0010
 Folate (μg/day)284 ± 100297 ± 99.90.0671
 Vitamin E (mg/day)10.6 ± 4.1211.2 ± 4.330.0879
 Mushroom (g/day)7.81 ± 9.9611.4 ± 21.20.0047
 Total vegetables (g/day)83.5 ± 16583.3 ± 88.50.9866
 Total fruits (g/day)312 ± 385278 ± 2460.1601

Table II shows some potential confounding factors by using the quintiles of daily mushroom intake. The prevalence of exercise (≥22.5 MET-hr/week) increased across quintiles of mushroom intake. Among the dietary factors, the intake of energy, soy protein, folate and vitamin E also increased across the quintiles of mushroom intake.

Table II. Selected Characteristics of Study Subjects According to the Quintiles of Dietary Mushroom Intake
 Quintiles of daily mushroom intakep for trend
1st (n = 145)2nd (n = 166)3rd (n = 134)4th (n = 88)5th (n = 191)
  1. All results are adjusted for age, and all nutrient consumptions are adjusted for total energy intake. Values are expressed as a Mean or Percent. p-values for the trends were determined by the general linear model for continuous variables and by the Cochran–Mantel–Haenszel test for categorical variables.

Median (g/day)02.454.909.8018.3 
Education (year)12121313130.0578
Body mass index (Kg/m2)24232323240.1893
Family history of breast cancer (%)27156.78.3110.1532
Current smoker (%)04.25.904.50.6786
Current alcohol drinker (%)48332642430.5981
Physical activity (≥22.5 MET-hr/week, %)10182411320.0023
Multivitamin user (%)1914181490.1558
Parity (%)89899393950.1922
Number of children2.22.02.12.02.20.3801
Oral contraceptive use (ever, %)1815157.3120.2419
Breast feeding (ever, %)76767473790.6702
Energy intake (kcal/day)1,8241,8902,0201,9892253<0.0001
Carbohydrate intake (g/day)3073213113143060.1445
Soy protein intake (g/day)8.37.38.97.29.90.0013
Folate intake (μg/day)268267287292343<0.0001
Vitamin E intake (mg/day)1010111113<0.0001

Table III shows the association between breast cancer risk and mushroom intake using quintiles of daily intake and quartiles of the average consumption frequency. A significant inverse association between breast cancer risk and mushroom intake was found in the last quantile for both the daily intake and the consumption frequency when compared to the lowest quantile of mushrooms (none or ≤0.53 g/day for daily intake and none or less than once per month for frequency). The inverse association of mushroom intake (OR = 0.55, 95% CI = 0.33–0.94 for daily intake; OR = 0.59, 95% CI = 0.37–0.94 for average consumption frequency) remained after adjusting for the potential confounders of the dietary nutrients intake (energy, carbohydrate, soy protein, vitamin E and folate), but the association in linear trends was no longer significant.

Table III. Odds Ratios (OR) and 95% Confidence Intervals (95% CI) of Breast Cancer by Quintiles of Mushroom Intake in Multivariate Models
Mushroom intakeMedian (min, max)No. of cases/controls (362/362)Multivariate adjusted OR (95% CI)1Multivariate adjusted OR (95% CI)2
  • 1

    Adjusted for education (year), family history of breast cancer (yes/no), regular exercise (≥22.5 MET-hr/week), BMI (Kg/m2), current smoker (yes/no), current drinker (yes/no), current multivitamin supplement (yes/no), number of children, menopausal status (pre/post) and energy (quintiles).

  • 2

    Adjusted for education (year), family history of breast cancer (yes/no), regular exercise (≥22.5 MET-hr/week), BMI (Kg/m2), current smoker (yes/no), current drinker (yes/no), current multivitamin supplement (yes/no), number of children, menopausal status (pre/post), energy (quintiles), carbohydrate (quintiles), soy protein (quintiles), vitamin E (quintiles) and folate (quintiles).

Daily intake (g/day)    
 Q10 (0, 0.53)91/541.00 (referent)1.00 (referent)
 Q22.45 (0.69, 2.80)80/860.53 (0.32–0.87)0.48 (0.28–0.81)
 Q34.90 (3.23, 5.60)62/720.56 (0.33–0.94)0.53 (0.30–0.92)
 Q49.80 (6.57, 13.8)46/420.66 (0.37–1.19)0.64 (0.34–1.18)
 Q518.3 (15.1, 245)83/1080.48 (0.30–0.78)0.55 (0.33–0.94)
 p for trend  0.02980.2690
 Continuous, 15 g/day  0.79 (0.65–0.97)0.84 (0.69–1.04)
Average frequency    
 Q1None (None, 0.91/month)119/841.00 (referent)1.00 (referent)
 Q22.4/month (1.0/month, 2.4/month)82/850.68 (0.43–1.07)0.68 (0.42–1.10)
 Q31.0/week (3.3/month, 2.9/week)72/730.74 (0.46–1.21)0.72 (0.43–1.20)
 Q43.0/week (3.0/week, 3.5/day)89/1200.54 (0.35–0.82)0.59 (0.37–0.94)
 p for trend  0.00820.0574
 Continuous, once/week  0.86 (0.78–0.95)0.88 (0.79–0.98)

Subjects were stratified according to menopausal status (235 premenopausal pairs and 127 postmenopausal pairs; Table IV) in order to evaluate the association in premenopausal and postmenopausal women. The premenopausal women showed an inverse association of cancer risk with both the daily intake, and the average consumption frequency of mushrooms after an adjustment for potential confounders without dietary factors (multivariate model 1) was made. Further adjustments for dietary factors, however, tended to attenuate these results in premenopausal women (OR = 0.44, 95% CI = 0.19–1.00 for daily intake; OR = 0.65, 95% CI = 0.34–1.26 for average frequency). Meanwhile, among postmenopausal women, the associations between mushroom intake and breast cancer risk were more apparent (OR = 0.16, 95% CI = 0.04–0.54 for daily intake; OR = 0.17, 95% CI = 0.05–0.54 for average consumption frequency). The inverse associations were also shown in the analyses with continuous data. The dose–response relationships were shown for both the daily intake of mushrooms (p for trend = 0.0190 in multivariate model 1 and p for trend = 0.0058 in multivariate model 2) and the average consumption frequency (p for trend = 0.0199 in multivariate model 1 and p for trend = 0.0037 in multivariate model 2).

Table IV. The Adjusted Odds Ratios (OR) and 95% Confidence Intervals (95% CI) of Mushroom Intake Stratified by Menopause Status in Relation to Breast Cancer Risk
Mushroom intakeMedian (min, max)No. of cases/controlsMultivariate adjusted OR (95% CI)1Multivariate adjusted OR (95% CI)2
  • 1

    Adjusted for education (year), family history of breast cancer (yes/no), regular exercise (≥22.5 MET-hr/week), BMI (Kg/m2), current smoker (yes/no), current drinker (yes/no), current multivitamin supplement (yes/no), number of children and energy (quintiles).

  • 2

    Adjusted for education (year), family history of breast cancer (yes/no), regular exercise (≥22.5 MET-hr/week), BMI (Kg/m2), current smoker (yes/no), current drinker (yes/no), current multivitamin supplement (yes/no), number of children, energy (quintiles), carbohydrate (quintiles), soy protein (quintiles), vitamin E (quintiles) and folate (quintiles).

Premenopausal women 235/235  
 Daily intake (g/day)    
  Q10 (0, 1.05)65/341.00 (referent)1.00 (referent)
  Q22.80 (1.17, 2.80)41/480.41 (0.21–0.81)0.38 (0.18–0.80)
  Q34.90 (3.23, 5.60)44/510.49 (0.25–0.98)0.51 (0.24–1.10)
  Q415.1 (7.53, 15.1)57/600.52 (0.28–0.97)0.60 (0.30–1.23)
  Q530.1 (17.5, 210)28/420.38 (0.19–0.77)0.44 (0.19–1.00)
  p for trend  0.06000.2726
  Continuous, 15 g/day  0.82 (0.64–1.04)0.88 (0.68–1.14)
 Average frequency    
  Q1None (None, 1.0/month)71/461.00 (referent)1.00 (referent)
  Q22.4/month (1.1/month, 3.6/month)59/590.73 (0.41–1.30)0.79 (0.42–1.49)
  Q31.0/week (1.0/week, 2.9/week)46/530.64 (0.34–1.22)0.62 (0.30–1.29)
  Q43.0/week (3.0/week, 3.5/day)59/770.57 (0.33–0.98)0.65 (0.34–1.26)
  p for trend  0.07160.3085
  Continuous, once/week  0.88 (0.78–0.99)0.90 (0.80–1.02)
Postmenopausal women 127/127  
 Daily intake (g/day)    
  Q10 (0, 0)38/281.00 (referent)1.00 (referent)
  Q21.85 (0.69, 2.45)19/160.91 (0.34–2.43)0.88 (0.24–3.21)
  Q33.23 (2.80, 5.02)18/290.38 (0.14–0.98)0.20 (0.05–0.71)
  Q47.96 (5.60, 13.8)28/180.78 (0.33–1.82)0.44 (0.14–1.38)
  Q515.1 (15.1, 245)24/360.29 (0.11–0.75)0.16 (0.04–0.54)
  p for trend  0.01900.0058
  Continuous, 15 g/day  0.72 (0.50–1.04)0.68 (0.45–1.03)
 Average frequency    
  Q1None (None, None)38/281.00 (referent)1.00 (referent)
  Q22.4/month (0.91/month, 2.4/month)34/370.62 (0.28–1.39)0.45 (0.16–1.32)
  Q31.0/week (3.3/month, 1.0/week)25/190.80 (0.33–1.95)0.46 (0.14–1.49)
  Q43.0/week (3.0/week, 3.5/day)30/430.35 (0.15–0.83)0.17 (0.05–0.54)
  p for trend  0.01990.0037
  Continuous, once/week  0.82 (0.68–0.99)0.79 (0.64–0.97)

Discussion

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Results
  5. Discussion
  6. Acknowledgements
  7. References

There is very limited evidence available regarding the associations between mushrooms and cancers in epidemiologic studies5, 13, 14 despite the anticancer effect of mushrooms in both in vitro5, 6, 7, 8, 9, 21 and in vivo5, 10, 22 assays. This is the reason why the associations between mushrooms and breast cancer among Korean women were investigated in this case–control study. The results from this study suggest that an inverse dose–response relationship exists between mushroom consumption and breast cancer risk in postmenopausal women.

The consumption of mushrooms has increased over the past several decades throughout the world, but Asians have been the major consumers of mushrooms for the past thousands of years as a source of nutrition and as medicine.2, 5, 16 According to the second Korean National Health and Nutrition Examination Survey (KNHANES, 2001),23 approximately 44% of Koreans had mushrooms at least once per week in 2001. The Lentinus edodes, Pleurotus ostreatus (Oyster mushroom) and Flammulina velutipes (Winter fungus) were most frequently consumed. The United States Department of Agriculture (USDA)24 reported that mushroom intake was 3.94 pounds (about 4.9 g/day) per capita in the U.S. in 2001 and among ethnic groups, the per capita use was highest among Asians [8.9 pounds (approximately 11.1 g/day)], whose consumption was more than twice the national average per capita. The average intake of mushrooms was 9.6 g/day in all of the women participants in this study (7.8 g/day in cases vs. 11.4 g/day in controls, p = 0.0036), which is similar to the average intake of Asians living in the U.S.24

There are only a few analytic epidemiologic studies on the association between mushrooms and cancer risk. A hospital-based case–control study13 in Korea concluded that there is a significant decrease in gastric cancer risk (p = 0.0003) with a higher mushroom intake. Another hospital-based case–control study in Japan14 reported marginal associations with gastric cancer risk only in the groups with the highest intake frequency (≥once/week) of Hypsizigus marmoreus (Bunashimeji) (OR = 0.57; 95% CI = 0.31–1.04) and Pholita nameko (Nameko) (OR = 0.56; 95% CI = 0.30–1.06). There was only 1 Korean study that focused on the beneficial effects of consuming mushrooms on breast cancer risk15; this study found that there is a decreased risk of breast cancer when mushroom consumption frequency is high (≥once/week) (OR = 0.4, 95% CI = 0.3–0.7). However, this finding is limited to only the dichotomized category of consumption frequency, because the study did not use the quantitative intake or the quantiles of mushroom intake to verify a dose–response. In the present study, the amount of mushroom intake and the consumption frequency data were used to show their associations with breast cancer risk in order to increase awareness and to provide more information about cancer prevention to the public. The results of this study indicated that an inverse dose–response relationship exists between mushroom intake and breast cancer in postmenopausal women. In light of the amounts and consumption frequency of mushrooms reported in this study, a consumption of at least 15.1 g of mushrooms per day or an intake of mushrooms at least 3 times per week could be beneficial for postmenopausal women. This assumption is based on the median values of the categories showing inverse associations of daily mushroom intake and the average frequency with breast cancer risk.

Mushrooms contain various biologically active compounds, such as phytochemicals, which have an inhibitory effect against oxidative stress,9 cell proliferation8 and the suppression of aromatase activity.10 Of these, the suppression of aromatase activity may explain why an inverse association was found in only postmenopausal women. Aromatase is thought to be an enzyme that converts androgens to local estrogens, which are major stimulatory factors for carcinogenesis of the breast among postmenopausal women.25 Recent studies have focused on aromatase inhibitors because of their chemopreventive properties, which may be preventative factors of breast cancer.26 Both in vivo and in vitro studies have found that mushrooms contain chemicals that can inhibit aromatase.6, 10, 27

Several limitations should be considered when interpreting the findings of this study. The first limitation is that while health-related behaviors such as regular exercise, smoking, drinking, multivitamin supplement use, BMI and dietary factors were adjusted for, the residual effects of other health-related behaviors may still have influenced the results. Given the common belief in Korea that mushrooms are healthy, people who preferred mushrooms would most likely have other healthy dietary habits.28, 29, 30 Another limitation of this study is the unfortunate inability to evaluate the impacts of commonly used commercial food products that contain mushroom components, including supplements, bottled drinks and home-made drinks derived from medicinal mushrooms (e.g., Ganoderma lucidum, Phellinus linteus).

In conclusion, increased dietary intake and consumption frequency of mushrooms may be associated, in a dose–response relationship, with a decreased risk of developing breast cancer in postmenopausal women. These findings may be helpful in providing recommendations to the public on how to prevent breast cancer, especially in postmenopausal women. Further studies on dietary mushrooms among various populations in a large cohort study are needed in order to generate more detailed guidelines about cancer prevention.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Results
  5. Discussion
  6. Acknowledgements
  7. References

Ms. M.K. Kim designed and supervised the execution of the study and Ms. S.A. Hong performed the analyses and wrote manuscript with Ms. K.R. Kim. Mr. S.J. Nam and Mr. G. Kong contributed to data preparation. All authors participated in the interpretation of the results and the editing of the manuscript.

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  3. Material and methods
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  5. Discussion
  6. Acknowledgements
  7. References
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