Nationwide Survey on Complementary and Alternative Medicine in Cancer Patients in Japan
http://www.100md.com
《临床肿瘤学》
the Medical Oncology Division and Surgical Oncology Division, National Shikoku Cancer Center, Matsuyama
Tokai University of Medicine, Isehara
Saitama Medical College, Saitama
Kyoto Prefectural University of Medicine, Kyoto
Kobe Pharmaceutical University, Kobe
National Cancer Center, Tokyo, Japan
ABSTRACT
PURPOSE: To determine the prevalence of use of complementary and alternative medicine (CAM) by patients with cancer in Japan, and to compare the characteristics of CAM users and CAM nonusers.
PATIENTS AND METHODS: A questionnaire on cancer CAM and the Hospital Anxiety and Depression Scale were delivered to 6,607 patients who were treated in 16 cancer centers and 40 palliative care units.
RESULTS: There were 3,461 available replies for a response rate of 52.4%. The prevalence of CAM use was 44.6% (1,382 of 3,100) in cancer patients and 25.5% (92 of 361) in noncancer patients with benign tumors. Multiple logistic regression analysis determined that history of chemotherapy, institute (palliative care units), higher education, an altered outlook on life after cancer diagnosis, primary cancer site, and younger age were strongly associated with CAM use in cancer patients. Most of the CAM users with cancer (96.2%) used products such as mushrooms, herbs, and shark cartilage. The motivation for most CAM use was recommendation from family members or friends (77.7%) rather than personal choice (23.3%). Positive effects were experienced by 24.3% of CAM users with cancer, although all of them received conventional cancer therapy concurrently. Adverse reactions were reported by 5.3% of cancer patients. CAM products were used without sufficient information by 57.3% of users with cancer and without a consultation with a doctor by 60.7% of users.
CONCLUSION: This survey revealed a high prevalence of CAM use among cancer patients, without sufficient information or consultation with their physicians. Oncologists should not ignore the CAM products used by their patients because of a lack of proven efficacy and safety.
INTRODUCTION
The WHO defines complementary and alternative medicine (CAM), or so-called traditional medicine, as follows: "a comprehensive term used to refer both to traditional medical systems such as traditional Chinese medicine, Indian ayurveda and Arabic unani medicine, and to various forms of indigenous medicine."1 CAM therapies include medication therapies (which involve the use of herbal medicine, animal parts, and/or minerals) and nonmedication therapies carried out primarily without the use of medication (such as acupuncture or manual therapy). Populations throughout Africa, Asia, and Latin America use traditional medicine to help meet their primary health care needs. In addition to being accessible and affordable, traditional medicine is also often part of a wider belief system, and is considered integral to everyday life and well-being. In Europe and North America, CAM is increasingly being used in parallel to allopathic medicine, particularly for treating and managing chronic disease. Concerns about the adverse effects of chemical medicines, a desire for more personalized health care, and greater public access to health information fuel the increasing use of CAM in many industrialized countries.2–5
The widespread use of a variety of nutritional, psychological, and natural medical approaches as CAM has been well documented.2,6–8 Recent surveys demonstrate that more than 50% of US cancer patients use CAM therapies at some point after their diagnosis.3,6,7 Despite extensive use, there is a paucity of data available to indicate whether these practices are efficacious and safe.9–11 Therefore, serious research efforts are underway to determine the scope of CAM use by patients and their motivations for its use.6–10 CAM in cancer medicine seems to be widely available in Japan as well as in the Western countries. We performed a preliminary survey on cancer CAM in a single cancer center in 1999. This survey revealed that 32% of cancer patients used CAM, and the most frequently used CAM involved natural products, such as mushrooms, shark cartilage, and beeswax-pollen mixtures.12 The most pressing and significant problems associated with these products were commonly held but incorrect assumptions and the absence of any regulatory oversight. In addition, interactions between herbs and drugs may increase or decrease the pharmacologic or toxicologic effects of either component. For example, St John's wort has recently been reported to dramatically reduce plasma levels of SN-38 (the active metabolite of irinotecan, a key oncologic drug), which may have a deleterious impact on treatment outcome.13
An enormous amount of unreliable information on cancer CAM is available from the Internet and other media sources. It is often the case that cancer patients and their relatives are at a loss about how to deal with such information and have a difficult time choosing what kind of CAM they should adopt. However, there have been no large-scale surveys of this sort in Asia, and the actual state of CAM use in cancer patients is still unclear. Therefore, we performed a nationwide cross-sectional survey to evaluate the prevalence of CAM use in cancer patients and their perceptions of cancer CAM, especially of CAM products used in Japan.
PATIENTS AND METHODS
Participants
Before initiation of this survey, the study protocol was examined by the institutional review boards of cancer centers and related hospitals (CCs) joining the nationwide association of medical centers for cancer and adult diseases in Japan, and hospice and palliative care units (PCUs) joining the Japanese association of palliative care. Sixteen of 29 CCs and 40 of 88 PCUs approved the survey. All participating institutions agreed not to treat patients systematically with any CAM. The total number of questionnaires that would be distributed to the patients was predicted by the responsible physician working for each collaborating institute, and this information was provided in advance to the National Shikoku Cancer Center. Questionnaires on cancer CAM were then sent to the responsible collaborating physicians in the CCs and PCUs from October 2001 to March 2002. The day on which the questionnaires were distributed to the patients was determined voluntarily by each institute within 2 weeks of receipt. Questionnaires were distributed to the patients by the medical staff (physicians, nurses, clerks, and so on) at each collaborating institute after exclusion of those with an Eastern Cooperative Oncology Group performance status of 4 and those who underwent surgery that day. Replies were sent back to the National Shikoku Cancer Center directly from each patient. Questionnaires were marked in advance to identify the type of clinic the patients were attending (ie, CCs or PCUs, and inpatient or outpatient). Returned questionnaires were coded with an identification number to ensure confidentiality.
Questionnaire
We had previously evaluated a questionnaire about cancer CAM in 219 cancer patients who were admitted to the National Shikoku Cancer Center as a preliminary study.12 In the present study, we used a modified version of that questionnaire after testing several samples. Some additional questions were quoted from previously published articles.6–8 The original questionnaire we used was written in Japanese. The attached questionnaire (Appendix) has been translated into English. The questionnaire was developed through a systematic literature review and discussions by two experienced medical oncologists, a psychiatrist, a pharmacist, a basic scientist, and a research assistant. On the cover page of the questionnaire, CAM was clearly defined as follows: "any therapy not included in the orthodox biomedical framework of care for patients. CAM means remedies that are used without the approval of the relevant government authorities, such as the Ministry of Health and Welfare in Japan, that approve new drugs after peer review of preclinical experiments and clinical trials regulated by law. CAM usually skips these steps and is offered directly to the public. Health insurance does not usually cover the cost of CAM, and patients will be liable for the whole expense incurred by any CAM. CAM includes natural products from mushrooms, herbs, green tea, shark cartilage, other special foods, megavitamins, acupuncture, aromatherapy, massage, meditation, and so on."
The questionnaire was composed of the following two parts: background of the patients (disease, onset, age, sex, daily living activity level, educational level, religion, cancer treatment, changes of outlook on life, satisfaction with receiving conventional medicine, and use of cancer CAM; questions 1 to 12) and users' perception of cancer CAM (initiation time, kinds of CAM used, reason for starting CAM, method of obtaining information about the CAM used, expectations for CAM use, effectiveness or ineffectiveness, adverse effects, average expense per month, whether a history of CAM use was provided to the physician in charge, whether the physician in charge was consulted, response of physician, reason for not consulting physician, and concurrent use of anticancer drugs and CAM products that are sold over the counter; questions 13 to 28).
Hospital Anxiety and Depression Scale
A brief scale, the Hospital Anxiety and Depression Scale (HADS), was used in this study to clarify the relationship between emotional state and CAM preference. The HADS has 14 items in two question groups, one each on anxiety and depression, and each question is rated from 0 to 3. The validity and reliability of the Japanese version of HADS have been confirmed previously.14,15 From previous articles, including the original one and studies in the Japanese population, we adopted 10 points as the cutoff above which anxiety and depression would be scored as high.14–16 The patients in the high group were considered to have an adjustment disorder or more severe condition. The HADS was delivered to patients along with the questionnaire on CAM.
Statistical Analysis
Differences of CAM use within categories of selected demographic and clinical variables (age, sex, disease sites, daily living activity level, patient's desire, changes of outlook on life, institute, education, and religion) were assessed by the 2 test. The factors predicting CAM use were analyzed by univariate analysis and then multiple logistic regression analysis was performed using all significant predictor variables (P < .05). The analysis provided an odds ratio and 95% CI for each variable while simultaneously controlling for the effects of other variables. Variables not contributing substantially to the model were systematically removed in a backward stepwise regression process using the likelihood ratio test as the criterion for removal. The Hosmer-Lemeshow 2 test was used to assess the goodness of fit between the observed and predicted number of outcomes for the final model, with P > .05 indicating a good fit. All analyses were performed using SPSS Base and Regression models 11.0J (SPSS Japan Inc, Tokyo, Japan)
RESULTS
Response Rate to Questionnaire and CAM User Rates
A total of 6,607 questionnaires on cancer CAM were sent to collaborating CCs and PCUs according to the required number estimated by the primary investigators at those institutes. As a result, questionnaires were delivered to 6,074 patients who were treated in CCs (2,688 inpatients and 3,386 outpatients) and to 533 patients who were treated in PCUs (367 inpatients and 166 outpatients). A total of 3,733 questionnaires were returned to our center, of which 3,461 were valid with useable answers. The remaining 272 returned questionnaires were invalid because of a critical lack of major answers, such as unwritten diagnosis or no response to CAM use. Consequently, the rate of valid replies was 52.4%. Of the valid replies, 3,100 were from cancer patients and 361 were from noncancer patients with benign tumors. The flow diagram of the study population is indicated in Figure 1.
The prevalence of CAM use in cancer patients was 44.6% (1,382 of 3,100) and that in noncancer patients was 25.5% (92 of 361). In terms of background differences, noncancer patients were younger, had less impaired daily activity, and were much more likely to be in CCs than cancer patients. The rate of use among cancer patients was significantly higher than that for noncancer patients (P < .0001). All of the 3,100 replies from cancer patients were subject to analysis. Many users (86.7%) started CAM after their diagnosis of cancer and 73.3% of users were continuing it at the time of the survey.
Backgrounds of Patients and CAM Users
The backgrounds of all the cancer patients and CAM users with cancer are summarized in Table 1. The prevalence of CAM use was significantly higher in patients who were younger than 61 years old (P < .0001), female (P < .0001), patients with a lower daily activity level (P < .0001), patients with higher education (P < .0001), patients who received chemotherapy (P < .0001), patients with a change of outlook on life (P < .0001), patients who were dissatisfied with conventional treatments (P = .0001), patients in PCUs (P < .0001), and patients with a low HADS anxiety score (P = .0029) and a high HADS depression score (P = .0049). In terms of disease sites, the rate of use was higher in patients with lung, breast, and hepatobiliary cancers than in those with other cancers (P < .0001). The prevalence of CAM use in inpatient wards of CCs and that in outpatient clinics of CCs was 40.6% and 45.3%, respectively. The prevalence of CAM users in inpatient wards of PCUs and that in outpatient clinics of PCUs was 61.0% and 64.3%, respectively. The prevalence of CAM use in PCUs was significantly higher than that in CCs in outpatient clinics (P < .0001), as well as inpatient wards (P < .0001). Similarly, the prevalence of CAM use in inpatient wards was significantly higher than that in outpatient clinics in both CCs (P < .0001) and PCUs (P < .0001).
Predictors of Cancer CAM Use
Multivariate logistic regression analysis was performed to detect the factors predictive of CAM use, using the variables with a significantly different rate among users. The institutional review board of one CC did not permit the questions about education and religion, and 500 questionnaires in which those two questions were deleted were sent to that center. As the result, the rate of reply on education and religion was apparently low. Given that the anxiety and depression scores of HADS could not be calculated if one of each of seven questions was not answered, the number of available replies was also decreased relative to the other questions. For these reasons we performed two analyses of the relevant variables separating the two patient populations: analysis 1 included the significant variables other than education and HADS, and analysis 2 included all significant variables as shown in Table 2. Patients who received chemotherapy; patients in PCUs; patients whose outlook on life had changed; patients with lung, breast, or hepatobiliary cancer; patients younger than 61 years old; and female patients were more likely to use CAM in both sets of analysis. In analysis 2, higher education was determined as a potent predictive factor, and dissatisfaction with conventional treatments was a weak predictive factor.
Types of CAM
The types of CAM used are listed in Table 3. The majority of CAM users (96.2%) relied on CAM products as opposed to nonmedical therapies. The most frequently used CAM product was mushrooms (Agaricus 60.6% and active hexose correlated compound [AHCC] 8.4%). Agaricus is extracted from a particular type of mushroom, Agaricus blazei Murill. It is purported to be an interferon inducer. AHCC is thought to act as an immunomodulator. Other CAM products were propolis (28.8%), Chinese herbs (7.1%), chitosan (7.1%), and shark cartilage (6.7%). Propolis is a beeswax-pollen mixture. Chitosan is an extract from crustaceans, such as crabs and lobsters. These are claimed to be enhancers of the immune system. Shark cartilage is known to be an inhibitor of tumor angiogenesis.17 Chinese herbs (easily bought over the counter, but not prescribed by physicians) were used by 7.1% of patients. The rate of use of traditional Chinese medicine (qigong, moxibustion, and acupuncture) was less than 4%.
Perceptions and Attitudes Toward CAM
As shown in Table 3, 77.7% of the patients started using CAM on recommendation from family members or friends. Only 23.3% of the patients decided to use CAM on the basis of their own will. Patients expected the following effects from CAM: suppression of tumor growth (67.1%), cure (44.5%), symptom relief (27.1%), and complementary effects to conventional therapy (20.7%). In terms of the effectiveness of CAM, 24.3% of the patients experienced positive effects, such as tumor shrinkage, inhibition of tumor growth, pain relief, fewer adverse effects from anticancer drugs, and feeling better. However, at the same time, all of the patients were treated with conventional therapies such as surgery, chemotherapy, hormonal therapy, and/or radiation. The effects were not related to the use of any specific CAM product. Almost two thirds of the patients did not know if the CAM really worked or not. Conversely, only 5.3% of the patients experienced adverse effects, such as nausea, diarrhea, constipation, skin eruption, and liver dysfunction. No adverse effects were experienced by 62.2% of the patients. Patients who were uncertain about adverse effects comprised 32.6% of respondents.
More than half of the patients (57.3%) started CAM without obtaining enough information on it. Most of the patients (84.5%) had not been asked about CAM use by their physician or other health professionals. Nearly two thirds of the patients (60.7%) have never consulted their physicians on CAM use. When the patients consulted their physicians, 60.3% of the patients were told that they were free to use it or not. Patients who were told to continue using CAM and those who were told to cease use comprised 10.5% (8.5% in CCs and 19.5% in PCUs) and 11.3% (12.2% in CCs and 7.3% in PCUs) of CAM users, respectively. The main reason (56.1%) given for why they were not willing to ask their physicians about CAM was that their physicians did not ask about CAM use. The prevalence of patients who thought the physicians would not understand CAM and who thought they would prohibit CAM use was 19.4% and 8.7%, respectively.
The prevalence of concurrent use of anticancer drugs and CAM products was 61.8% in CAM users. The average monthly expenditure for CAM was 57,000 yen (approximately US $500; range, 0 to 1200,000 yen).
DISCUSSION
The surveyed cancer population in this study used complementary but not alternative therapies because they were simultaneously treated in conventional medical facilities. However, we could not completely rule out the possibility that they had previously used alternative medicine. Therefore, we used the term CAM in this study.
Although we received more than 3,000 replies, the response rate (52.4%) was a little lower than in previous studies.3,6,18,19 This may have introduced bias into our study. However, the patients' privacy was completely preserved and our survey method was the easiest way for the patients to reply to the questionnaire without feeling any pressure. We believe that our survey is helpful for assessing regional research priorities and for comparing the current status of CAM use in studies using a similar mailed-questionnaire method in other countries.
The prevalence of CAM use in cancer patients was significantly higher than that in noncancer patients. Most of the noncancer patients in this study had benign tumors and attended the cancer centers. Therefore, the noncancer patients in our study represent neither the general healthy population nor patients with benign chronic disease. Indeed, the rate of CAM use in the general population of people suffering from disease in our country was reported to be higher than that of our noncancer patients.20 The prevalence of CAM use in cancer patients was 44.6%. This rate was slightly higher than that found in our previous study (32%) of a single cancer center survey.12 The prevalence appears to increase each year in our country, as in the Western countries.2 CAM user rates were significantly higher in patients undergoing chemotherapy and in patients in PCUs, and these associations were confirmed by multivariate analysis. Chemotherapy is usually delivered to inoperable, advanced, or metastatic cancers with a palliative intent but not a curative intent. In PCUs, there were no conventional treatments with tumor shrinkage as the expected outcome. Patients' relatives or friends often recommended that the patient use CAM products in that situation. In general, medical professionals in PCUs are rather generous in accepting the use of CAM. The percentage of patients whose CAM use had been recommended was approximately two-fold higher in PCUs (19.5%) compared with that in CCs (8.5%). These are probably the primary reasons for the high rate of CAM use in patients undergoing chemotherapy and in PCUs. The multivariate analysis also revealed a close association between CAM use and high educational status, changes in outlook on life, primary cancer site, and younger age. The patients' perception of received conventional treatments and female sex were marginal predictors in our study. Predictors of CAM use have been reported in many previous studies,7,8,19 and our data support that these predictors are similar to those in developed countries. With few exceptions, the literature indicates that highly educated patients and younger patients tend to use CAM.
Different predictors are associated with the different types of CAM used. In our surveyed population, the most frequently used CAM was natural products. Oral intake of medications is more likely in patients with lung, breast, and hepatobiliary cancers than in patients with head and neck, GI, and urogenital cancers, taking the sites of disease and the manners of progression into consideration. This is likely to be closely related to the use of CAM products because all of these are oral supplements. The predictors chemotherapy and disease site would therefore be related to the type of CAM used (ie, CAM products). Indeed, this hypothesis was suggested in a previous report in which predictors shifted to include chemotherapy after spirituality and psychotherapy or support groups were excluded from the types of CAM used.7 Supplements (herbs or vitamins) were the main types of CAM used by the patients of that limited analysis. Unexpectedly, psychological factors such as anxiety and depression showed no relation to the use of CAM. However, these factors frequently fluctuate during the disease course, as we observed in the process of informed consent.15 If the HADS had been administered when the patients initiated CAM use, the results would likely be different.
The majority of CAM users in this study took products such as mushrooms, herbs, and shark cartilage. Mushrooms (Agaricus and AHCC) were the most frequently used among the products. This was characteristic of our CAM users. The popular types of CAM in Western countries, such as spiritual practice, mind and body therapy, vitamins and special diet, and homeopathy, were rarely used in our country. Such mushrooms are sold in Japan as diet supplements. The providers emphasize their effects on boosting the immune system based on basic experimental findings using cultured human tumor cells, and advertise in many magazines or through the Internet with anecdotal reports of users. No reliable, well-designed clinical trials in cancer patients have been performed with these mushrooms. Nonetheless, many cancer patients used such products hoping for tumor growth suppression (67.1%) and cure (44.5%) rather than complementary effects (20.7%). These mushrooms and other similar natural products are generally expensive. This contributed to the high expenditure on CAM among our users (US $500 per month on average), compared with that in the Western countries (US $50 to $70 per month on average).6 The main motive for CAM use was the recommendation of family members or friends. The population of patients who were willing to seek out CAM on their own was unexpectedly small, about one fourth of the users. It has been reported that support group dynamics influence individuals to be more likely to use CAM among breast cancer survivors.6 In our study, many patients seemed to be motivated to use CAM by the recommendations of relatives. Friends also offered recommendations on CAM use.
Approximately one fourth of the users experienced positive effects from CAM, even though they all received conventional therapies previously or concurrently. Although it was unclear whether the positive effects were due to the CAM products or the conventional treatments, they nonetheless believed that the CAM was effective. In retrospect, we should have added a question to our questionnaire about the effectiveness of the conventional treatments received. Conversely, most patients reported no adverse reactions to CAM. However, the potential for harmful drug-CAM product interactions exists.21–23 Herbs or vitamins can mask or distort the effects of conventional drugs.
This survey revealed that approximately 60% of users started CAM without obtaining enough information about it, and without informing their doctors. This proportion was similar to that in our previous survey.12 The same issues have been pointed out in many reports from the United States and Europe.7,24,25 In our survey, when patients consulted their physicians, 60.3% of the patients were told that they were free to continue using CAM or to stop, whereas 10.5% of the patients were told to continue using CAM and 11.3% of the patients were told to stop. These figures were also similar to the results in our previous study of clinical oncologists.26 When oncologists were asked, 74% of them neither recommended nor prohibited the use of the products. Twelve percent of them encouraged their patients to use CAM products, and 6% told their patients to stop. It appears that a difficult situation for many oncologists emerges because of the lack of scientific information on CAM. However, physicians should acknowledge that the main reason (56.1%) patients did not inform their physicians of their CAM use was that the physicians did not ask them about it. These results indicate that better patient-physician communication and more reliable information on CAM products are needed. The prevalence of concurrent use of anticancer drugs and CAM products was considerably high (61.8%) in the present study. In our previous survey of oncologists, 83.9% of oncologists had administered anticancer drugs concurrently with CAM products.12 Nevertheless, our present knowledge of interactions is incomplete, especially regarding anticancer drugs.22,23 More research is urgently needed. Oncologists should be aware of these facts, and the use of CAM products should be determined before initiating chemotherapy, especially when using new investigational drugs.
A few limitations of this study must be acknowledged. First, the response rate was somewhat low compared with that of other studies, although it was greater than 50%, as discussed previously. Second, there is no definite evidence that our study population is representative of cancer patients in Japan. It seems impossible to select cancer patients randomly from throughout the entire country. We used the associations of CCs and PCUs in Japan as our survey source. Otherwise, such a large-scale survey could not be performed. These limitations have also been reported in the previous literature,7,8 and unfortunately, inconsistencies in measures of CAM and differing patient populations and methodologies (ie, interviews v mailed surveys) limit the generalization of studies on CAM use.3,4 Third, two questions were deleted from the questionnaire sent to one of the CCs. As a result, about 500 replies on education and religion were lacking. However, the analyses with or without the data from that center achieved similar results. Therefore, this did not significantly affect our conclusions.
Many cancer patients continue receiving oncologic care with standard therapies while pursuing CAM methods. A recent survey regarding the impact of the media and the Internet on cancer patients revealed that 71% of cancer patients actively searched for information, and 50% used the Internet.27 The survey concluded that strategic efforts were needed to provide guidance for patients to help them better interpret such medical information. Oncologists need to be aware of the importance of this issue and of the rationale used to promote CAM. A great need for public and professional education regarding this subject is evident.
Authors' Disclosures of Potential Conflicts of Interest
The authors indicated no potential conflicts of interest.
Appendix
Acknowledgment
We thank all of the physicians and patients who participated in this survey.
NOTES
Supported by a Grant-in-Aid (13-20) for Cancer Research from the Ministry of Health, Labor and Welfare, Japan.
Authors' disclosures of potential conflicts of interest are found at the end of this article.
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Cassileth BR: Complementary and alternative cancer medicine. J Clin Oncol 17:44-52, 1999
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Yamashita H, Tsukayama H, Sugishita C: Popularity of complementary and alternative medicine in Japan: A telephone survey. Complement Ther Med 10:84-93, 2002
Matthews HB, Lucier GW, Fisher KD: Medicinal herbs in the United States: Research needs. Environ Health Perspect 107:773-778, 1999
Ernst E: Herb-drug interactions: Potentially important but woefully under-researched. Eur J Clin Pharmacol 56:523-524, 2000
Marcus DM, Grollman AP: Botanical medicines: The need for new regulations. N Engl J Med 347:2073-2076, 2002
Risberg T, Lund E, Wist E, et al: Cancer patients use of nonproven therapy: A 5-year follow-up study. J Clin Oncol 16:6-12, 1998
Burstein HJ: Discussing complementary therapies with cancer patients: What should we be talking about J Clin Oncol 18:2501-2504, 2000
Hyodo I, Eguchi K, Nishina T, et al: Perceptions and attitudes of clinical oncologists on complementary and alternative medicine: A nationwide survey in Japan. Cancer 97:2861-2868, 2003
Chen X, Siu LL: Impact of the media and the internet on oncology: Survey of cancer patients and oncologists in Canada. J Clin Oncol 19:4291-4297, 2001(Ichinosuke Hyodo, Noriko )
Tokai University of Medicine, Isehara
Saitama Medical College, Saitama
Kyoto Prefectural University of Medicine, Kyoto
Kobe Pharmaceutical University, Kobe
National Cancer Center, Tokyo, Japan
ABSTRACT
PURPOSE: To determine the prevalence of use of complementary and alternative medicine (CAM) by patients with cancer in Japan, and to compare the characteristics of CAM users and CAM nonusers.
PATIENTS AND METHODS: A questionnaire on cancer CAM and the Hospital Anxiety and Depression Scale were delivered to 6,607 patients who were treated in 16 cancer centers and 40 palliative care units.
RESULTS: There were 3,461 available replies for a response rate of 52.4%. The prevalence of CAM use was 44.6% (1,382 of 3,100) in cancer patients and 25.5% (92 of 361) in noncancer patients with benign tumors. Multiple logistic regression analysis determined that history of chemotherapy, institute (palliative care units), higher education, an altered outlook on life after cancer diagnosis, primary cancer site, and younger age were strongly associated with CAM use in cancer patients. Most of the CAM users with cancer (96.2%) used products such as mushrooms, herbs, and shark cartilage. The motivation for most CAM use was recommendation from family members or friends (77.7%) rather than personal choice (23.3%). Positive effects were experienced by 24.3% of CAM users with cancer, although all of them received conventional cancer therapy concurrently. Adverse reactions were reported by 5.3% of cancer patients. CAM products were used without sufficient information by 57.3% of users with cancer and without a consultation with a doctor by 60.7% of users.
CONCLUSION: This survey revealed a high prevalence of CAM use among cancer patients, without sufficient information or consultation with their physicians. Oncologists should not ignore the CAM products used by their patients because of a lack of proven efficacy and safety.
INTRODUCTION
The WHO defines complementary and alternative medicine (CAM), or so-called traditional medicine, as follows: "a comprehensive term used to refer both to traditional medical systems such as traditional Chinese medicine, Indian ayurveda and Arabic unani medicine, and to various forms of indigenous medicine."1 CAM therapies include medication therapies (which involve the use of herbal medicine, animal parts, and/or minerals) and nonmedication therapies carried out primarily without the use of medication (such as acupuncture or manual therapy). Populations throughout Africa, Asia, and Latin America use traditional medicine to help meet their primary health care needs. In addition to being accessible and affordable, traditional medicine is also often part of a wider belief system, and is considered integral to everyday life and well-being. In Europe and North America, CAM is increasingly being used in parallel to allopathic medicine, particularly for treating and managing chronic disease. Concerns about the adverse effects of chemical medicines, a desire for more personalized health care, and greater public access to health information fuel the increasing use of CAM in many industrialized countries.2–5
The widespread use of a variety of nutritional, psychological, and natural medical approaches as CAM has been well documented.2,6–8 Recent surveys demonstrate that more than 50% of US cancer patients use CAM therapies at some point after their diagnosis.3,6,7 Despite extensive use, there is a paucity of data available to indicate whether these practices are efficacious and safe.9–11 Therefore, serious research efforts are underway to determine the scope of CAM use by patients and their motivations for its use.6–10 CAM in cancer medicine seems to be widely available in Japan as well as in the Western countries. We performed a preliminary survey on cancer CAM in a single cancer center in 1999. This survey revealed that 32% of cancer patients used CAM, and the most frequently used CAM involved natural products, such as mushrooms, shark cartilage, and beeswax-pollen mixtures.12 The most pressing and significant problems associated with these products were commonly held but incorrect assumptions and the absence of any regulatory oversight. In addition, interactions between herbs and drugs may increase or decrease the pharmacologic or toxicologic effects of either component. For example, St John's wort has recently been reported to dramatically reduce plasma levels of SN-38 (the active metabolite of irinotecan, a key oncologic drug), which may have a deleterious impact on treatment outcome.13
An enormous amount of unreliable information on cancer CAM is available from the Internet and other media sources. It is often the case that cancer patients and their relatives are at a loss about how to deal with such information and have a difficult time choosing what kind of CAM they should adopt. However, there have been no large-scale surveys of this sort in Asia, and the actual state of CAM use in cancer patients is still unclear. Therefore, we performed a nationwide cross-sectional survey to evaluate the prevalence of CAM use in cancer patients and their perceptions of cancer CAM, especially of CAM products used in Japan.
PATIENTS AND METHODS
Participants
Before initiation of this survey, the study protocol was examined by the institutional review boards of cancer centers and related hospitals (CCs) joining the nationwide association of medical centers for cancer and adult diseases in Japan, and hospice and palliative care units (PCUs) joining the Japanese association of palliative care. Sixteen of 29 CCs and 40 of 88 PCUs approved the survey. All participating institutions agreed not to treat patients systematically with any CAM. The total number of questionnaires that would be distributed to the patients was predicted by the responsible physician working for each collaborating institute, and this information was provided in advance to the National Shikoku Cancer Center. Questionnaires on cancer CAM were then sent to the responsible collaborating physicians in the CCs and PCUs from October 2001 to March 2002. The day on which the questionnaires were distributed to the patients was determined voluntarily by each institute within 2 weeks of receipt. Questionnaires were distributed to the patients by the medical staff (physicians, nurses, clerks, and so on) at each collaborating institute after exclusion of those with an Eastern Cooperative Oncology Group performance status of 4 and those who underwent surgery that day. Replies were sent back to the National Shikoku Cancer Center directly from each patient. Questionnaires were marked in advance to identify the type of clinic the patients were attending (ie, CCs or PCUs, and inpatient or outpatient). Returned questionnaires were coded with an identification number to ensure confidentiality.
Questionnaire
We had previously evaluated a questionnaire about cancer CAM in 219 cancer patients who were admitted to the National Shikoku Cancer Center as a preliminary study.12 In the present study, we used a modified version of that questionnaire after testing several samples. Some additional questions were quoted from previously published articles.6–8 The original questionnaire we used was written in Japanese. The attached questionnaire (Appendix) has been translated into English. The questionnaire was developed through a systematic literature review and discussions by two experienced medical oncologists, a psychiatrist, a pharmacist, a basic scientist, and a research assistant. On the cover page of the questionnaire, CAM was clearly defined as follows: "any therapy not included in the orthodox biomedical framework of care for patients. CAM means remedies that are used without the approval of the relevant government authorities, such as the Ministry of Health and Welfare in Japan, that approve new drugs after peer review of preclinical experiments and clinical trials regulated by law. CAM usually skips these steps and is offered directly to the public. Health insurance does not usually cover the cost of CAM, and patients will be liable for the whole expense incurred by any CAM. CAM includes natural products from mushrooms, herbs, green tea, shark cartilage, other special foods, megavitamins, acupuncture, aromatherapy, massage, meditation, and so on."
The questionnaire was composed of the following two parts: background of the patients (disease, onset, age, sex, daily living activity level, educational level, religion, cancer treatment, changes of outlook on life, satisfaction with receiving conventional medicine, and use of cancer CAM; questions 1 to 12) and users' perception of cancer CAM (initiation time, kinds of CAM used, reason for starting CAM, method of obtaining information about the CAM used, expectations for CAM use, effectiveness or ineffectiveness, adverse effects, average expense per month, whether a history of CAM use was provided to the physician in charge, whether the physician in charge was consulted, response of physician, reason for not consulting physician, and concurrent use of anticancer drugs and CAM products that are sold over the counter; questions 13 to 28).
Hospital Anxiety and Depression Scale
A brief scale, the Hospital Anxiety and Depression Scale (HADS), was used in this study to clarify the relationship between emotional state and CAM preference. The HADS has 14 items in two question groups, one each on anxiety and depression, and each question is rated from 0 to 3. The validity and reliability of the Japanese version of HADS have been confirmed previously.14,15 From previous articles, including the original one and studies in the Japanese population, we adopted 10 points as the cutoff above which anxiety and depression would be scored as high.14–16 The patients in the high group were considered to have an adjustment disorder or more severe condition. The HADS was delivered to patients along with the questionnaire on CAM.
Statistical Analysis
Differences of CAM use within categories of selected demographic and clinical variables (age, sex, disease sites, daily living activity level, patient's desire, changes of outlook on life, institute, education, and religion) were assessed by the 2 test. The factors predicting CAM use were analyzed by univariate analysis and then multiple logistic regression analysis was performed using all significant predictor variables (P < .05). The analysis provided an odds ratio and 95% CI for each variable while simultaneously controlling for the effects of other variables. Variables not contributing substantially to the model were systematically removed in a backward stepwise regression process using the likelihood ratio test as the criterion for removal. The Hosmer-Lemeshow 2 test was used to assess the goodness of fit between the observed and predicted number of outcomes for the final model, with P > .05 indicating a good fit. All analyses were performed using SPSS Base and Regression models 11.0J (SPSS Japan Inc, Tokyo, Japan)
RESULTS
Response Rate to Questionnaire and CAM User Rates
A total of 6,607 questionnaires on cancer CAM were sent to collaborating CCs and PCUs according to the required number estimated by the primary investigators at those institutes. As a result, questionnaires were delivered to 6,074 patients who were treated in CCs (2,688 inpatients and 3,386 outpatients) and to 533 patients who were treated in PCUs (367 inpatients and 166 outpatients). A total of 3,733 questionnaires were returned to our center, of which 3,461 were valid with useable answers. The remaining 272 returned questionnaires were invalid because of a critical lack of major answers, such as unwritten diagnosis or no response to CAM use. Consequently, the rate of valid replies was 52.4%. Of the valid replies, 3,100 were from cancer patients and 361 were from noncancer patients with benign tumors. The flow diagram of the study population is indicated in Figure 1.
The prevalence of CAM use in cancer patients was 44.6% (1,382 of 3,100) and that in noncancer patients was 25.5% (92 of 361). In terms of background differences, noncancer patients were younger, had less impaired daily activity, and were much more likely to be in CCs than cancer patients. The rate of use among cancer patients was significantly higher than that for noncancer patients (P < .0001). All of the 3,100 replies from cancer patients were subject to analysis. Many users (86.7%) started CAM after their diagnosis of cancer and 73.3% of users were continuing it at the time of the survey.
Backgrounds of Patients and CAM Users
The backgrounds of all the cancer patients and CAM users with cancer are summarized in Table 1. The prevalence of CAM use was significantly higher in patients who were younger than 61 years old (P < .0001), female (P < .0001), patients with a lower daily activity level (P < .0001), patients with higher education (P < .0001), patients who received chemotherapy (P < .0001), patients with a change of outlook on life (P < .0001), patients who were dissatisfied with conventional treatments (P = .0001), patients in PCUs (P < .0001), and patients with a low HADS anxiety score (P = .0029) and a high HADS depression score (P = .0049). In terms of disease sites, the rate of use was higher in patients with lung, breast, and hepatobiliary cancers than in those with other cancers (P < .0001). The prevalence of CAM use in inpatient wards of CCs and that in outpatient clinics of CCs was 40.6% and 45.3%, respectively. The prevalence of CAM users in inpatient wards of PCUs and that in outpatient clinics of PCUs was 61.0% and 64.3%, respectively. The prevalence of CAM use in PCUs was significantly higher than that in CCs in outpatient clinics (P < .0001), as well as inpatient wards (P < .0001). Similarly, the prevalence of CAM use in inpatient wards was significantly higher than that in outpatient clinics in both CCs (P < .0001) and PCUs (P < .0001).
Predictors of Cancer CAM Use
Multivariate logistic regression analysis was performed to detect the factors predictive of CAM use, using the variables with a significantly different rate among users. The institutional review board of one CC did not permit the questions about education and religion, and 500 questionnaires in which those two questions were deleted were sent to that center. As the result, the rate of reply on education and religion was apparently low. Given that the anxiety and depression scores of HADS could not be calculated if one of each of seven questions was not answered, the number of available replies was also decreased relative to the other questions. For these reasons we performed two analyses of the relevant variables separating the two patient populations: analysis 1 included the significant variables other than education and HADS, and analysis 2 included all significant variables as shown in Table 2. Patients who received chemotherapy; patients in PCUs; patients whose outlook on life had changed; patients with lung, breast, or hepatobiliary cancer; patients younger than 61 years old; and female patients were more likely to use CAM in both sets of analysis. In analysis 2, higher education was determined as a potent predictive factor, and dissatisfaction with conventional treatments was a weak predictive factor.
Types of CAM
The types of CAM used are listed in Table 3. The majority of CAM users (96.2%) relied on CAM products as opposed to nonmedical therapies. The most frequently used CAM product was mushrooms (Agaricus 60.6% and active hexose correlated compound [AHCC] 8.4%). Agaricus is extracted from a particular type of mushroom, Agaricus blazei Murill. It is purported to be an interferon inducer. AHCC is thought to act as an immunomodulator. Other CAM products were propolis (28.8%), Chinese herbs (7.1%), chitosan (7.1%), and shark cartilage (6.7%). Propolis is a beeswax-pollen mixture. Chitosan is an extract from crustaceans, such as crabs and lobsters. These are claimed to be enhancers of the immune system. Shark cartilage is known to be an inhibitor of tumor angiogenesis.17 Chinese herbs (easily bought over the counter, but not prescribed by physicians) were used by 7.1% of patients. The rate of use of traditional Chinese medicine (qigong, moxibustion, and acupuncture) was less than 4%.
Perceptions and Attitudes Toward CAM
As shown in Table 3, 77.7% of the patients started using CAM on recommendation from family members or friends. Only 23.3% of the patients decided to use CAM on the basis of their own will. Patients expected the following effects from CAM: suppression of tumor growth (67.1%), cure (44.5%), symptom relief (27.1%), and complementary effects to conventional therapy (20.7%). In terms of the effectiveness of CAM, 24.3% of the patients experienced positive effects, such as tumor shrinkage, inhibition of tumor growth, pain relief, fewer adverse effects from anticancer drugs, and feeling better. However, at the same time, all of the patients were treated with conventional therapies such as surgery, chemotherapy, hormonal therapy, and/or radiation. The effects were not related to the use of any specific CAM product. Almost two thirds of the patients did not know if the CAM really worked or not. Conversely, only 5.3% of the patients experienced adverse effects, such as nausea, diarrhea, constipation, skin eruption, and liver dysfunction. No adverse effects were experienced by 62.2% of the patients. Patients who were uncertain about adverse effects comprised 32.6% of respondents.
More than half of the patients (57.3%) started CAM without obtaining enough information on it. Most of the patients (84.5%) had not been asked about CAM use by their physician or other health professionals. Nearly two thirds of the patients (60.7%) have never consulted their physicians on CAM use. When the patients consulted their physicians, 60.3% of the patients were told that they were free to use it or not. Patients who were told to continue using CAM and those who were told to cease use comprised 10.5% (8.5% in CCs and 19.5% in PCUs) and 11.3% (12.2% in CCs and 7.3% in PCUs) of CAM users, respectively. The main reason (56.1%) given for why they were not willing to ask their physicians about CAM was that their physicians did not ask about CAM use. The prevalence of patients who thought the physicians would not understand CAM and who thought they would prohibit CAM use was 19.4% and 8.7%, respectively.
The prevalence of concurrent use of anticancer drugs and CAM products was 61.8% in CAM users. The average monthly expenditure for CAM was 57,000 yen (approximately US $500; range, 0 to 1200,000 yen).
DISCUSSION
The surveyed cancer population in this study used complementary but not alternative therapies because they were simultaneously treated in conventional medical facilities. However, we could not completely rule out the possibility that they had previously used alternative medicine. Therefore, we used the term CAM in this study.
Although we received more than 3,000 replies, the response rate (52.4%) was a little lower than in previous studies.3,6,18,19 This may have introduced bias into our study. However, the patients' privacy was completely preserved and our survey method was the easiest way for the patients to reply to the questionnaire without feeling any pressure. We believe that our survey is helpful for assessing regional research priorities and for comparing the current status of CAM use in studies using a similar mailed-questionnaire method in other countries.
The prevalence of CAM use in cancer patients was significantly higher than that in noncancer patients. Most of the noncancer patients in this study had benign tumors and attended the cancer centers. Therefore, the noncancer patients in our study represent neither the general healthy population nor patients with benign chronic disease. Indeed, the rate of CAM use in the general population of people suffering from disease in our country was reported to be higher than that of our noncancer patients.20 The prevalence of CAM use in cancer patients was 44.6%. This rate was slightly higher than that found in our previous study (32%) of a single cancer center survey.12 The prevalence appears to increase each year in our country, as in the Western countries.2 CAM user rates were significantly higher in patients undergoing chemotherapy and in patients in PCUs, and these associations were confirmed by multivariate analysis. Chemotherapy is usually delivered to inoperable, advanced, or metastatic cancers with a palliative intent but not a curative intent. In PCUs, there were no conventional treatments with tumor shrinkage as the expected outcome. Patients' relatives or friends often recommended that the patient use CAM products in that situation. In general, medical professionals in PCUs are rather generous in accepting the use of CAM. The percentage of patients whose CAM use had been recommended was approximately two-fold higher in PCUs (19.5%) compared with that in CCs (8.5%). These are probably the primary reasons for the high rate of CAM use in patients undergoing chemotherapy and in PCUs. The multivariate analysis also revealed a close association between CAM use and high educational status, changes in outlook on life, primary cancer site, and younger age. The patients' perception of received conventional treatments and female sex were marginal predictors in our study. Predictors of CAM use have been reported in many previous studies,7,8,19 and our data support that these predictors are similar to those in developed countries. With few exceptions, the literature indicates that highly educated patients and younger patients tend to use CAM.
Different predictors are associated with the different types of CAM used. In our surveyed population, the most frequently used CAM was natural products. Oral intake of medications is more likely in patients with lung, breast, and hepatobiliary cancers than in patients with head and neck, GI, and urogenital cancers, taking the sites of disease and the manners of progression into consideration. This is likely to be closely related to the use of CAM products because all of these are oral supplements. The predictors chemotherapy and disease site would therefore be related to the type of CAM used (ie, CAM products). Indeed, this hypothesis was suggested in a previous report in which predictors shifted to include chemotherapy after spirituality and psychotherapy or support groups were excluded from the types of CAM used.7 Supplements (herbs or vitamins) were the main types of CAM used by the patients of that limited analysis. Unexpectedly, psychological factors such as anxiety and depression showed no relation to the use of CAM. However, these factors frequently fluctuate during the disease course, as we observed in the process of informed consent.15 If the HADS had been administered when the patients initiated CAM use, the results would likely be different.
The majority of CAM users in this study took products such as mushrooms, herbs, and shark cartilage. Mushrooms (Agaricus and AHCC) were the most frequently used among the products. This was characteristic of our CAM users. The popular types of CAM in Western countries, such as spiritual practice, mind and body therapy, vitamins and special diet, and homeopathy, were rarely used in our country. Such mushrooms are sold in Japan as diet supplements. The providers emphasize their effects on boosting the immune system based on basic experimental findings using cultured human tumor cells, and advertise in many magazines or through the Internet with anecdotal reports of users. No reliable, well-designed clinical trials in cancer patients have been performed with these mushrooms. Nonetheless, many cancer patients used such products hoping for tumor growth suppression (67.1%) and cure (44.5%) rather than complementary effects (20.7%). These mushrooms and other similar natural products are generally expensive. This contributed to the high expenditure on CAM among our users (US $500 per month on average), compared with that in the Western countries (US $50 to $70 per month on average).6 The main motive for CAM use was the recommendation of family members or friends. The population of patients who were willing to seek out CAM on their own was unexpectedly small, about one fourth of the users. It has been reported that support group dynamics influence individuals to be more likely to use CAM among breast cancer survivors.6 In our study, many patients seemed to be motivated to use CAM by the recommendations of relatives. Friends also offered recommendations on CAM use.
Approximately one fourth of the users experienced positive effects from CAM, even though they all received conventional therapies previously or concurrently. Although it was unclear whether the positive effects were due to the CAM products or the conventional treatments, they nonetheless believed that the CAM was effective. In retrospect, we should have added a question to our questionnaire about the effectiveness of the conventional treatments received. Conversely, most patients reported no adverse reactions to CAM. However, the potential for harmful drug-CAM product interactions exists.21–23 Herbs or vitamins can mask or distort the effects of conventional drugs.
This survey revealed that approximately 60% of users started CAM without obtaining enough information about it, and without informing their doctors. This proportion was similar to that in our previous survey.12 The same issues have been pointed out in many reports from the United States and Europe.7,24,25 In our survey, when patients consulted their physicians, 60.3% of the patients were told that they were free to continue using CAM or to stop, whereas 10.5% of the patients were told to continue using CAM and 11.3% of the patients were told to stop. These figures were also similar to the results in our previous study of clinical oncologists.26 When oncologists were asked, 74% of them neither recommended nor prohibited the use of the products. Twelve percent of them encouraged their patients to use CAM products, and 6% told their patients to stop. It appears that a difficult situation for many oncologists emerges because of the lack of scientific information on CAM. However, physicians should acknowledge that the main reason (56.1%) patients did not inform their physicians of their CAM use was that the physicians did not ask them about it. These results indicate that better patient-physician communication and more reliable information on CAM products are needed. The prevalence of concurrent use of anticancer drugs and CAM products was considerably high (61.8%) in the present study. In our previous survey of oncologists, 83.9% of oncologists had administered anticancer drugs concurrently with CAM products.12 Nevertheless, our present knowledge of interactions is incomplete, especially regarding anticancer drugs.22,23 More research is urgently needed. Oncologists should be aware of these facts, and the use of CAM products should be determined before initiating chemotherapy, especially when using new investigational drugs.
A few limitations of this study must be acknowledged. First, the response rate was somewhat low compared with that of other studies, although it was greater than 50%, as discussed previously. Second, there is no definite evidence that our study population is representative of cancer patients in Japan. It seems impossible to select cancer patients randomly from throughout the entire country. We used the associations of CCs and PCUs in Japan as our survey source. Otherwise, such a large-scale survey could not be performed. These limitations have also been reported in the previous literature,7,8 and unfortunately, inconsistencies in measures of CAM and differing patient populations and methodologies (ie, interviews v mailed surveys) limit the generalization of studies on CAM use.3,4 Third, two questions were deleted from the questionnaire sent to one of the CCs. As a result, about 500 replies on education and religion were lacking. However, the analyses with or without the data from that center achieved similar results. Therefore, this did not significantly affect our conclusions.
Many cancer patients continue receiving oncologic care with standard therapies while pursuing CAM methods. A recent survey regarding the impact of the media and the Internet on cancer patients revealed that 71% of cancer patients actively searched for information, and 50% used the Internet.27 The survey concluded that strategic efforts were needed to provide guidance for patients to help them better interpret such medical information. Oncologists need to be aware of the importance of this issue and of the rationale used to promote CAM. A great need for public and professional education regarding this subject is evident.
Authors' Disclosures of Potential Conflicts of Interest
The authors indicated no potential conflicts of interest.
Appendix
Acknowledgment
We thank all of the physicians and patients who participated in this survey.
NOTES
Supported by a Grant-in-Aid (13-20) for Cancer Research from the Ministry of Health, Labor and Welfare, Japan.
Authors' disclosures of potential conflicts of interest are found at the end of this article.
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