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Psychosomatic Medicine 67:72-77 (2005)
© 2005 American Psychosomatic Society

ORIGINAL ARTICLES

Perceived Psychologic Stress and Colorectal Cancer Mortality: Findings From the Japan Collaborative Cohort Study

Masayo Kojima, MD, PhD, Kenji Wakai, MD, PhD, Shinkan Tokudome, MD, PhD, Koji Tamakoshi, MD, PhD, Hideaki Toyoshima, MD, PhD, Yoshiyuki Watanabe, MD, PhD, Norihiko Hayakawa, MD, PhD, Koji Suzuki, PhD, Shuji Hashimoto, PhD, Miyuki Kawado, MSc, Sadao Suzuki, MD, PhD, Yoshinori Ito, PhD and Akiko Tamakoshi, MD, PhD for the JACC Study Group

From the Department of Health Promotion and Preventive Medicine, Nagoya City University Graduate School of Medical Sciences, Nagoya, Japan (M.K., S.T., S.S.); the Division of Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya, Japan (K.W.); the Department of Preventive Medicine/Biostatistics and Medical Decision Making, Nagoya University Graduate School of Medicine, Nagoya, Japan (K.W., A.T.); the Department of Public Health/Health Information Dynamics, Nagoya University Graduate School of Medicine, Nagoya, Japan (K.T., H.T.); the Department of Epidemiology for Community Health and Medicine, Kyoto Prefectural University of Medicine Graduate School of Medical Science, Kyoto, Japan (Y.W.); the Department of Epidemiology, Research Institute for Radiation Biology and Medicine, Hiroshima University, Hiroshima, Japan (N.H.); the Department of Public Health, Fujita Health University School of Health Sciences, Aichi, Japan (K.S., Y.I.); and the Department of Hygiene, Fujita Health University School of Medicine, Aichi, Japan (S.H., M.K.).

Address correspondence and reprint requests to Masayo Kojima, MD, PhD, Department of Health Promotion and Preventive Medicine, Nagoya City University Graduate School of Medical Sciences, 1 Kawasumi, Mizuho-cho, Mizuho-ku, Nagoya 467-8601, Japan. E-mail: masayok{at}med.nagoya-cu.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 
Objective: The purpose of this research was to examine the relationship between perceived psychologic stress and colorectal cancer mortality in a prospective large-scale study.

Methods: Between the years 1988 and 1990, 32,153 men and 45,854 women aged 40 to 79 years were enrolled. Participants completed a self-administered questionnaire that addressed demographic, lifestyle, and psychosocial characteristics. Subjects were subsequently followed for mortality until the end of 1999. Perceived psychologic stress was assessed using the question "Do you feel stress during your daily life?" The 4 possible responses, ranging from "little or none" (1) to "extreme" (4), were dichotomized as low (1 or 2) or high (3 or 4) stress. Relative risks (RRs) with 95% confidence intervals (CIs) for colon and rectal cancer according to the perceived level of stress were estimated using Cox’s proportional hazard model.

Results: During the follow-up period (average, 9.6 years), 193 colon cancer deaths (96 men and 97 women) and 127 rectal cancer deaths (88 men and 39 women) were confirmed within the study group. Women who reported high stress had a 1.64-fold higher risk of colon cancer mortality (multivariate-adjusted RR, 1.64; 95% CI, 1.01–2.66) compared with those reporting low stress. There was no significant association between perceived stress and female rectal cancer or male colon and rectal cancer mortality.

Conclusions: Perceived psychologic stress was weakly associated with increased mortality from colon cancer in women. No positive or inverse association was found in men. Further studies are needed to confirm our results.

Key Words: colorectal carcinoma • psychosocial factors • perceived stress • cohort study

Abbreviations: BMI = body mass index; CI = confidence interval; HPA axis = hypothalamic–pituitary–adrenocortical axis; ICD-10 = 10th Revision of the International Classification of Diseases; OR = odds ratio; RR = relative risk; SAM system = sympathetic–adrenal–medullary system.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 
Thehuman body responds to stress through the autonomic nervous system, the hypothalamic–pituitary–adrenocortical (HPA) axis and the cardiovascular, metabolic, and immune systems. However, the physiological systems that are activated by stress can themselves cause damage (1). According to Rosch (2), the idea that cancer might be related to stress or emotional factors is as old as the history of medicine. Many clinical and laboratory studies, as well as anecdotal reports, support the hypothesis that stress can significantly influence susceptibility and resistance to cancer, and can affect the course of the disease (2–4). However, epidemiologic studies have produced inconsistent results, largely owing to inappropriate study design and the difficulties measuring psychologic variables (5). Dalton et al. (6) reviewed the data from previous epidemiologic studies and found no association between major life events and cancer risk, and inconsistent conclusions were obtained with respect to depression and personality factors. The authors attributed these inconclusive results to methodologic weaknesses in the studies such as inadequacies in sample size, length of follow up, the detection of cancer cases, and control for confounding factors. This highlights the need for well-designed large prospective studies of the association between cancer risk and psychologic variables.

Colorectal cancer is the second leading cause of cancer-related death in most developed countries (7). Epidemiologic studies have revealed that several lifestyle factors such as a diet rich in fat but poor in vegetables and fiber combined with low physical activity increase the risk of colorectal cancer (8). Alcohol intake (9) and constipation (10,11) have also been suggested to increase the risk. The colon and rectum are known to be particularly sensitive to psychologic stress (12–15), and lifestyle factors and behaviors that are associated with colorectal cancer risk are also influenced by psychologic stress (1,16). Some case–control studies have reported a positive association between colorectal cancer risk and psychosocial stress factors such as job-related stress (17,18) and stressful life events (19,20). However, because having cancer itself is a stressful event, it is difficult for patients to accurately evaluate previous stressful events and their psychologic status without recall bias. Such biases could be avoided by examining the relationship between these factors in a prospective study.

Stress can be defined as a nonspecific response of the body to a demand from the environment or as a process of adaptation in reaction to psychologic, physical, or chemical stimuli. There are unlimited sources of stress, and responses vary greatly between individuals and in different situations (16,21). The way in which an individual perceives a situation determines their specific response to stressful stimuli (1). Common physiological responses to stress are alterations of the sympathetic–adrenal–medullary (SAM) system and the HPA axis. Both the autonomic nervous system and the HPA axis can, in turn, influence the immune system, and persistent suppression of the immune system increases the risk of cancer. More specifically, dysfunction of the autonomic nervous system might cause irregular bowel movements, which have recently been identified as a possible risk factor for colon cancer (22).

We therefore propose that individuals who experience high levels of perceived stress during their daily life are at a greater risk of mortality from colorectal cancer. To test this hypothesis, we evaluated the perceived levels of psychologic stress in healthy Japanese adults. The subjects were then followed prospectively to examine the association between psychologic stress and colorectal cancer death. Adjustments were made during analysis of the data for possible confounding factors.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 
The Japan Collaborative Cohort Study for Evaluation of Cancer Risk
All data were taken from the Japan Collaborative Cohort Study for Evaluation of Cancer Risk (JACC Study), which was a nationwide multicenter collaborative study sponsored by the Ministry of Education, Culture, Sports, Science and Technology of Japan (Monbukagakusho). The methods of the JACC Study have been described in detail elsewhere (23). Briefly, the original study population consisted of 110,792 Japanese adults aged 40 to 79, who were enrolled between the years 1988 and 1990 in 45 areas throughout Japan. Most of the subjects were recruited from the general population or when undergoing routine health checks in the municipalities. On enrollment, participants completed a self-administered questionnaire that assessed demographic characteristics, lifestyle habits, and medical history, as well as psychologic attitudes toward life. Written informed consent for participation was obtained individually from subjects, with the exception of those in a few study areas in which informed consent was provided at the group level after the aim of the study and confidentiality of the data had been explained to community leaders. The study protocol was approved by the Ethics Committee of Medical Care and Research of Fujita Health University School of Medicine, Japan.

The focus of this study was the association between psychologic stress and colorectal cancer. We therefore excluded 73 individuals who reported a history of colorectal cancer, along with all of the respondents from the six areas in which the questionnaire did not include the psychologic evaluation section (n = 23,330). In addition, those who neglected to address this section (n = 7511) and those who did not answer the specific question about psychologic stress (n = 1867) were excluded; 10.7% of the eligible participants refused to answer this question. A total of 78,007 subjects (32,153 men and 45,854 women) were therefore included in the final analysis.

Evaluation of Perceived Psychologic Stress
Perceived psychologic stress was assessed in this study through responses to the question "Do you feel stress during your daily life?" Four possible answers were provided: little or none (1), moderate (2), high (3), and extreme (4). For the purposes of the analysis, these responses were dichotomized and subjects who chose response 1 or 2 were categorized as having high stress levels, whereas those that chose response 3 or 4 were categorized as having low stress levels.

Identification of Colorectal Cancer Cases and Follow Up of the Cohort
Subjects were followed for mortality until the end of 1999. The Family Registration Law in Japan requires registration of death. Therefore, mortality was determined using municipal resident registration records, and causes of death were confirmed using death certificates, with permission from the Ministry of Public Management, Home Affairs, Post and Telecommunications. The end point of the study was defined as death from colon cancer (International Classification of Diseases, 10th Revision [ICD-10]: C18) or rectal cancer (ICD-10: C20). Subjects who moved out of the study area or died from causes other than colorectal cancer were treated as censored cases. During the study period, only 3.3% (n = 2600) of the participants were lost from the follow up as a result of change of residence. We calculated the risk period for each subject as the interval between the date of questionnaire administration and whichever of the following occurred first: the date of death or the date of moving from the study area or December 31, 1999.

Statistical Analysis
Although colon and rectal cancers are often considered together, several differences have been identified in their etiologies (24). We therefore separately evaluated the risk of colon cancer and rectal cancer by sex. All analyses were performed using the SAS statistical package, release 8.2 (SAS Inc., Cary, NC).

First, to explore the background characteristics of psychologic stress, we calculated the means and proportions of the baseline variables for each level of perceived psychologic stress by gender. Mean values were compared using analysis of covariance with adjustment for age. The relationships between the baseline categorical variables and psychologic stress were examined using logistic regression, with adjustment for age, by gender; significant interactions between gender and baseline variables in relation to psychologic stress were further examined through logistic regression models. Then, to determine the impact of perceived psychologic stress on colorectal cancer mortality, age-adjusted relative risks (RR) with 95% confidence intervals (CIs) for colon and rectal cancers according to the perceived level of stress were estimated using Cox’s proportional hazard model. We calculated the RRs for "high" versus "low" stress levels and tested for linear trends in the associations by including the responses as continuous variables. To adjust for the influence of possible confounding factors, multivariate adjusted models were computed. The first model included the following age and lifestyle factors, which are known to influence colorectal cancer risk: body mass index (BMI) calculated as weight (kg)/height (m2) and categorized as "≥25 kg/m2" or "<25 kg/m2;" history of colorectal cancer in parents or siblings ("yes" or "no"); current smoking status ("smoker" or "nonsmoker"); intake frequency of alcohol ("≥5 days per week" or "<5 days per week"); sleep duration per night ("<7 hours" or "≥7 hours"); intake frequency of green leafy vegetables ("daily" or "not daily"); time spent walking per day ("≤30 minutes" or ">30 minutes"); and severe constipation (bowel movement frequency "once every 4 days or less" or "once every 3 days or more"). All of the variables of the baseline characteristics were then added to the second model, which included the following sociologic factors: age at leaving full-time education ("≥20 years" or "<20 years"); marital status ("married" or "unmarried"); having children ("yes" or "no"); and being in full-time employment ("yes" or "no").

For each covariate, missing values were treated as an additional category in the variables and were included in the models. In all cases, two-sided probability (p) values <.05 were considered to be statistically significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 NOTES
 REFERENCES
 
During the follow-up period (average, 9.6 years; standard deviation, 2.0 years; total of 749,354 person-years), a total of 7685 deaths (4563 men and 3122 women) were recorded, which included 193 deaths from colon cancer (96 men and 97 women) and 127 deaths from rectal cancer (88 men and 39 women).

Table 1 presents the baseline characteristics of the study population for each level of perceived psychologic stress. Significant gender interactions were observed for all variables, with the exceptions of marital status and family history. Regardless of sex, subjects who reported high stress were more likely to be married than those who reported low stress, although this trend was only weakly significant. Stress was more strongly associated with younger age, higher education levels, having a full-time job, and having fewer hours of sleep per day in men compared with women. Daily consumption of green leafy vegetables was negatively associated with stress in men, but not in women. Having children and having a BMI ≥25 kg/m2 were both inversely associated with stress in women, but not men. In addition, smoking, daily alcohol consumption, and severe constipation were all positively associated with stress in women alone.


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  		TABLE 1. Background Characteristics at Baseline of the Participants by Perceived Stress by Gender

 

Next, the impacts of perceived psychologic stress on colon and rectal cancer mortalities were estimated by gender, using Cox’s proportional hazard model (Table 2). In men, there was no significant association between perceived psychologic stress and colon or rectal cancer mortality; the age-adjusted RRs were 1.01 (95% CI, 0.58–1.75) for colon cancer and 0.93 (95% CI, 0.52–1.66) for rectal cancer. These results were almost unchanged by adjustment for possible confounding factors. In women, a marginally significant association was found between the dichotomized levels of perceived psychologic stress and colon cancer mortality. Women who reported high psychologic stress had a 1.61-fold higher mortality risk (95% CI, 1.00–2.61) compared with those who reported low stress. This risk increased slightly after adjustment for lifestyle factors (multivariate adjusted RR1, 1.64; 95% CI, 1.01–2.66). Even after adjusting for all of the baseline characteristics, including sociologic factors, the association between stress and female colon cancer remained significant (RR2, 1.63; 95% CI, 1.002–2.640). The RR for rectal cancer mortality associated with perceived high psychologic stress in women was also greater than unity, although this relationship was not statistically significant (age-adjusted RR, 1.28; 95% CI, 0.59–2.81; multivariate adjusted RR1, 1.27; 95% CI, 0.58–2.80; RR2, 1.27; 95% CI, 0.58–2.81). No linear trend was observed between response to the stress question and colon or rectal cancer mortality in either men or women.


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  		TABLE 2. Relative Risk (RR) for Colorectal Cancer Mortality According to the Level of Perceived Stress, Derived From Cox’s Proportional Hazard Models by Genderm

 


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
NOTES
 REFERENCES
 
We found a weak but significant positive association between perceived psychologic stress and the risk of female colon cancer mortality. An increased risk of rectal cancer mortality was also observed in women, although the association was not statistically significant. No positive or inverse association was found between perceived psychologic stress and colon and rectal cancer mortality in men.

The strength of our study lies in the fact that we evaluated the baseline characteristics of all subjects when they were free from cancer and then followed them prospectively. In addition, our subjects were members of the general population recruited from a total of 45 different communities from across Japan. This study design significantly limited the influence of both recall and selection biases, which are unavoidable in case–control studies.

Iso et al. examined the relationship between perceived stress and mortality from cardiovascular diseases in the same initial population as the present study using a similar questionnaire (25). Their analysis revealed positive associations between perceived stress and increased stroke mortality in women, and between perceived stress and chronic heart disease in both sexes. Lifestyle factors that are associated with colorectal cancer risk—such as obesity, low physical activity, excessive alcohol consumption, and low vegetable intake—are also known risk factors for cardiovascular diseases. However, even when we adjusted for these factors in our analysis, the independent association between colon cancer mortality and perceived psychologic stress persisted in women. These observations indicate that for both female colon cancer and cardiovascular diseases, psychologic stress is possibly an independent risk factor separate from other lifestyle factors.

Colorectal cancer and psychologic stress were not positively associated among the male subjects in our study. Numerous epidemiologic studies have reported an increased prevalence of stress-related disorders—including acute stress disorder, posttraumatic stress disorder, and major depressive disorder—among women compared with men. However, we cannot conclude from our data alone that men are less susceptible than women to the effects of stress in relation to colorectal cancer risk. We observed significant gender interactions between most of the background characteristics examined and perceived stress levels. High stress was more strongly associated in men than in women with having a full-time job, and spending less time sleeping and walking. Having children and obesity were both inversely associated; by contrast, smoking and daily alcohol consumption were positively associated with stress in women alone. Although we adjusted for all of these variables in our multivariate analysis, it remains possible that a combination of perceived psychologic stress and differences in background characteristics might increase the risk of female colon cancer. We should also note that limitations of the questionnaire might provide an alternative explanation for the gender differences observed in the present study. The single question that was used to assess perceived stress levels might not have accurately reflected the psychologic burden of male subjects. Further studies will be necessary to clarify gender differences in the relationship between perceived psychologic stress and colorectal cancer risk.

Female sex hormones might have a role in the association between stress and colon cancer risk. It has been suggested that colon cancer might share etiologic factors with breast cancer in women (26,27). A number of studies have shown protective effects of parity on cancers of the colon, breast, and reproductive organs (28); modifications of hormone profiles caused by pregnancy and their effects on bile acid metabolism might be the main mechanisms of these associations (29,30). Recently, Helgesson et al. examined a cohort of 1462 Swedish women aged 38 to 60 years and followed these subjects for 24 years (31). The authors reported that stress associated with daily activities, which was measured using a four-item self-administered questionnaire, was associated with a twofold increase in the risk of subsequent breast cancer compared with individuals that reported no stress. Although the possible mechanisms of this association have not been addressed, the interaction between psychologic stress and female sex hormones in relation to cancer risk is worthy of further investigation.

Some limitations to the interpretation of our data should be noted. First, the end point of the study was death from colon or rectal cancer, so the risks reported here relate to fatal colon and rectal cancers only, not cancers that respond to curative treatments. Moreover, these data do not allow a discussion of whether perceived psychologic stress influences the development or progression of colorectal cancers. Second, perceived stress was assessed only on the basis of the response to a single question: "Do you feel stress during your daily life?" Stress is clearly a complex phenomenon, the measurement of which is controversial, and it is not possible to capture full data on this subject using any available tools at present. However, it is generally agreed that the reliability of a test increases with the number of questions (32). Our findings should therefore be confirmed using more sophisticated methods to assess psychologic stress from a range of perspectives, including general and specific types of stress that are related to different environments such as the home and workplace.

Third, although we observed a significant association between the dichotomized levels of stress and the risk of female colon cancer, there was no linear trend between the four separate responses to the stress question and colon cancer mortality. These data do not allow us to determine whether there is an acceptable level of perceived stress or whether the results are the result of limitations of the questionnaire.

In conclusion, perceived psychologic stress was weakly associated with increased mortality from colon cancer in women but not in men. Future studies should attempt to clarify these results in terms of gender differences and their relevance to other types of cancer. In addition, it will be important to explore the most appropriate methods of measuring stress in the context of its role as a possible risk factor for cancer.

The authors express their sincere appreciation to Dr. K Aoki, Professor Emeritus, Nagoya University School of Medicine, and the former chairman of the JACC Study Group, and Dr. H Sugano, the former Director of the Cancer Institute of the Japanese Foundation for Cancer Research, who greatly contributed to the initiation of the study.

The present members of the JACC Study and their affiliations are as follows: Dr. A. Tamakoshi (present chairman of the study group), Nagoya University Graduate School of Medicine; Dr. M. Mori, Sapporo Medical University School of Medicine; Dr. Y. Motohashi, Akita University School of Medicine; Dr. I. Tsuji, Tohoku University Graduate School of Medicine; Dr. Y. Nakamura, Jichi Medical School; Dr. H. Iso, Institute of Community Medicine, University of Tsukuba; Dr. H. Mikami, Chiba Cancer Center; Dr. Y. Inaba, Juntendo University School of Medicine; Dr. Y. Hoshiyama, Showa University School of Medicine; Dr. H. Suzuki, Niigata University Graduate School of Medical and Dental Sciences; Dr. H. Shimizu, Gifu University School of Medicine; Dr. H. Toyoshima, Nagoya University Graduate School of Medicine; Dr. S. Tokudome, Nagoya City University Graduate School of Medical Science; Dr. Y. Ito, Fujita Health University School of Health Sciences; Dr. S. Hashimoto, Fujita Health University School of Medicine; Dr. Shogo Kikuchi, Aichi Medical University School of Medicine; Dr. A. Koizumi, Graduate School of Medicine and Faculty of Medicine, Kyoto University; Dr. T. Kawamura, Kyoto University Center for Student Health; Dr. Y. Watanabe and Dr. Tsuneharu Miki, Kyoto Prefectural University of Medicine Graduate School of Medical Science; Dr. C. Date, Faculty of Human Environmental Sciences, Mukogawa Women’s University; Dr. K. Sakata, Wakayama Medical University; Dr. T. Nose, Tottori University Faculty of Medicine; Dr. Norihiko Hayakawa, Research Institute for Radiation Biology and Medicine, Hiroshima University; Dr. T. Yoshimura, Institute of Industrial Ecological Sciences, University of Occupational and Environmental Health, Japan; Dr. K. Fukuda, Kurume University School of Medicine; Dr. N. Okamoto, Kanagawa Cancer Center; Dr. H. Shio, Moriyama Municipal Hospital; Dr. Y. Ohno (former chairman of the study group), Asahi Rosai Hospital; Dr. T. Kitagawa, Cancer Institute of the Japanese Foundation for Cancer Research; Dr. T. Kuroki, Gifu University; and Dr. Kazuo Tajima, Aichi Cancer Center Research Institute.

The past members of the study, other than the following seven members, were listed in reference 23 (affiliations are those at the time of study participation): Dr. T. Shimamoto, Institute of Community Medicine, University of Tsukuba; Dr. H. Tanaka, Medical Research Institute, Tokyo Medical and Dental University; Dr. S. Hisamichi, Tohoku University Graduate School of Medicine; Dr. M. Nakao, Kyoto Prefectural University of Medicine; Dr. T. Suzuki, Research Institute, Osaka Medical Center for Cancer and Cardiovascular Diseases; Dr. T. Hashimoto, Wakayama Medical University; and Dr. T. Ishibashi, Asama General Hospital.


   NOTES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 NOTES
REFERENCES
 
This work was supported by a Grant-in-Aid for Scientific Research on Priority Areas (2; No. 14031222) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. The JACC Study has also been supported by Grants-in-Aid for Scientific Research from the same ministry (Nos. 61010076, 62010074, 63010074, 1010068, 2151065, 3151064, 4151063, 5151069, 6279102, and 11181101).

Received for publication February 8, 2004; revision received July 21, 2004.

DOI:10.1097/01.psy.0000151742.43774.6d


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 

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E. D. Kirby, V. P. Williams, M. C. Hocking, J. D. Lane, and R. B. Williams
Psychosocial Benefits of Three Formats of a Standardized Behavioral Stress Management Program
Psychosom Med, November 1, 2006; 68(6): 816 - 823.
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