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© 2000 American Society for Clinical Oncology Complementary/Alternative Medicine Use in a Comprehensive Cancer Center and the Implications for OncologyFrom the Centers for Alternative Medicine Research and Health Promotion Research and Development, The University of Texas-Houston School of Public Health; Departments of Biostatistics and Surgical Oncology, The University of Texas M.D. Anderson Cancer Center; and Section of Health Services Research, Baylor College of Medicine, Houston, TX. Address reprint requests to Mary Ann Richardson, DrPH, National Institutes of Health, National Center for Complementary and Alternative Medicine, 31 Center Dr, Room 5B-58, Bethesda, MD 20892-2182; email marich@ od.nih.gov.
PURPOSE: Oncologists are aware that their patients use complementary/alternative medicine (CAM). As cancer incidence rates and survival time increase, use of CAM will likely increase. This study assessed the prevalence and predictors of CAM use in a comprehensive cancer center.
SUBJECTS AND METHODS: Subjects were English-speaking cancer patients at least 18 years of age, attending one of eight outpatient clinics at The University of Texas M.D. Anderson Cancer Center, Houston, TX, between December 1997 and June 1998. After giving written informed consent, participants completed a self-administered questionnaire. Differences between CAM users and nonusers were assessed by RESULTS: Of the 453 participants (response rate, 51.4%), 99.3% had heard of CAM. Of those, 83.3% had used at least one CAM approach. Use was greatest for spiritual practices (80.5%), vitamins and herbs (62.6%), and movement and physical therapies (59.2%) and predicted (P < .001) by sex (female), younger age, indigent pay status, and surgery. After excluding spiritual practices and psychotherapy, 95.8% of participants were aware of CAM and 68.7% of those had used CAM. Use was predicted (P < .0001) by sex (female), education, and chemotherapy. CONCLUSION: In most categories, CAM use was common among outpatients. Given the number of patients combining vitamins and herbs with conventional treatments, the oncology community must improve patient-provider communication, offer reliable information to patients, and initiate research to determine possible drug-herb-vitamin interactions.
THE POPULARITY OF complementary/alternative medicine (CAM) is an international phenomenon. The prevalence of CAM use is estimated at 25% among residents of the United Kingdom,1 50% among German, French,1 and Australian2 populations, and 42% to 69% among residents of the United States.3,4 CAM is a major growth industry in Europe,5,6 and that trend is now mirrored in the United States, where out-of-pocket expenditures for CAM in 1997 were estimated at $34.4 billion.3 In the United States between 1990 and 1997, the prevalence of CAM use increased from 33.8% to 42.1%, and the number of visits to CAM practitioners increased from 427 million to 629 million visits.3 A summary of 26 surveys across 13 countries concluded that the prevalence of CAM use by cancer patients overall was 31.4% (range, 7% to 64%).7 Most cancer patients combine CAM with conventional therapy.8-10 The typical CAM user in the United States is reported to be white, more affluent, better educated, 30 to 50 years of age, and living in the western or northeastern regions of the country.10-12 National surveys in the 1980s and early 1990s reported that metabolic, dietary, and megavitamin approaches,11 imagery, and electronic treatments10 were the most popular approaches. Oncologists are becoming increasingly aware that patients use CAM, yet few oncologists discuss these therapies with patients.13-15 Instead, the established medical community is demanding regulation and evaluation of CAM.16,17 Some groups insist that CAM poses serious health risks and cite poor outcomes for patients who reject proven conventional cancer treatment for CAM approaches.18,19 The increasing interest in CAM among cancer patients may be due to limitations of conventional cancer treatment, increased advertising and media coverage of CAM, or the desire for holistic or natural treatments. Cancer patients want more information,13 and some patients believe access to CAM should be part of standard cancer treatment.20 As cancer incidence increases and survival time lengthens, the population seeking information about and access to CAM is likely to increase. Information on CAM use in comprehensive cancer centers is limited and outdated. Although we acknowledge that use of these therapies is common, information on contemporary use, attitudes, and beliefs is needed for clinicians, program planners, and patient educators who must respond to the growing interest among patients, particularly in the comprehensive cancer centers. The purpose of this study was to examine CAM use in a more current, representative sample of cancer outpatients. Specifically, this study assessed (1) prevalence of CAM use among cancer patients at a comprehensive cancer center; (2) characteristics of the CAM users, including demographic, disease, and treatment variables; (3) reasons for CAM use; and (4) level of interest among patients for information about CAM.
English-speaking cancer patients who were at least 18 years of age and reported to one of eight outpatient clinics (breast, thoracic/head and neck, gastrointestinal, urology, prostate, melanoma/sarcoma, gynecology, and lymphoma) at M.D. Anderson Cancer Center between December 1997 and June 1998 were invited to participate in the study. Between 50 and 100 outpatients from each clinic were accrued for the study after written informed consent was obtained. The study was approved by the institutional review board at M.D. Anderson. Nurse coordinators at each outpatient clinic provided the research assistants with a daily schedule of patients who registered for clinic appointments. After patients signed in at the clinic, the research assistants introduced the study—describing it as a survey to learn about CAM use—and then determined patient eligibility. As part of the consent process, patients were informed that they could withdraw from the study at any time and skip any survey question. To increase accuracy, patients recorded their responses directly onto the questionnaire. Questionnaires were returned to a research assistant and coded with a unique identification number to ensure confidentiality. Research assistants attempted to contact every patient in the clinic. They maintained a daily record of the accrual process, including the number of patients who could not be screened for eligibility because of the busy clinic environment and of those screened, the reasons for ineligibility and nonparticipation.
Questionnaire CAM therapies were classified into seven major categories: (1) special diets, including vegetarian, vegan, macrobiotic, and Gerson diets; (2) psychotherapy with a social worker, psychologist, psychiatrist, or support group; (3) movement and physical therapy, including exercise, yoga, tai chi or chi gong, chiropractic or osteopathic manipulation, and massage; (4) mind/body therapies, including imagery or visualization, hypnosis, meditation, biofeedback, energy healing or therapeutic touch, journaling, and music therapy; (5) spiritual practices, including prayer for self and prayer/spiritual healing by others; (6) vitamins and herbs, including melatonin, essiac, mistletoe, laetrile, shark or bovine cartilage, homeopathy, and ayurvedic and folk remedies; and (7) other approaches (ie, immuno-augmentative treatment, 714X, cancell, bioelectromagnetic therapy, and acupuncture). Patients who had discussed CAM therapies with providers were asked to describe the response of their providers; other patients were asked about reasons for not discussing CAM with their providers. In addition, patients were asked to describe where they obtained information about CAM (eg, books, physicians, nurses) and their interest in receiving additional information. Patients who expressed an interest in learning more about CAM therapies were asked their preferred sources for information.
Measures
Statistical Analysis
Candidate variables were entered into a multivariate logistic regression model to assess their relationship with CAM use. The model provided an odds ratio (OR) and 95% confidence interval (CI) for each variable while simultaneously controlling for the effect of other variables. The OR is a statistical estimate of the probability of observing an association between the variable of interest, and the 95% CI provides a measure of precision for the estimate. Variables not contributing substantially to the model were systematically removed in a backwards stepwise regression process using the likelihood ratio test as the criterion for removal. The Hosmer-Lemeshow
Eligibility and Consent Rate A total of 1,671 patients signed into the clinics during the study period; however, a total of 280 patients were never identified for screening after signing in at the clinic, 310 patients were identified but left for their appointment before being screened for eligibility, and 37 patients left the clinic before being called for their appointment or screened by the research staff. Therefore, a total of 1,044 patients were available and screened for eligibility by the research staff, and 882 (84.5%) were eligible for participation. Of the 162 patients who were ineligible, reasons for exclusion included the following: no cancer diagnosis (n = 60), younger than 18 years of age (n = 16), unable to speak English (n = 67), and unable to participate because of medical problems (n = 19). Of the 882 eligible patients, 493 consented to participate and completed the survey. A total of 40 patients consented to participate but were later excluded because they did not complete (n = 10) or return (n = 30) the questionnaire. The final sample consisted of 453 outpatients (response rate, 51.4%) from the following clinics: breast (n = 60), melanoma/skin cancer (n = 56), lymphoma (n = 57), gynecologic (n = 56), gastrointestinal (n = 58), genitourinary (n = 114), and thoracic/head and neck (n = 52). Continuous variables were approximately normally distributed.
After patients who participated were separated from those who refused to participate, Specifically, younger patients (ie, < 55 years of age) were 2.1 times (95% CI, 1.6 to 2.9) more likely to participate than older patients. Those who had an ability to pay their medical bills (ie, full or partial medical coverage) were 1.7 times (95% CI, 1.1 to 2.8) more likely to participate than those who were indigent, and patients treated at the breast clinic were 1.9 times (95% CI, 1.1 to 3.3) more likely to participate than those presenting at all of the other clinics combined.
Patterns of CAM Use
Patients were asked to identify the two CAM therapies they used most often. The most popular therapies among those who responded (n = 226) were vitamins and herbs (41.9%), spiritual practices (35.5%), and mind/body approaches (10.1%). From a list of 39 possible CAM therapies, the average number of CAM therapies used by patients (n = 374) was 4.8 (SD, 3.7; median, four; range, one to 23) or 3.7 therapies (SD, 3.1; median, three; range, one to 18) when excluding spirituality and psychotherapy/group support (Table 2).
Predictors of CAM Use Preliminary comparisons by  2 analyses suggested that CAM users and nonusers did not differ with respect to ethnicity, marital status, religious affiliation, level of education, place of residence, disease characteristics, and prior or pending treatment. However, users differed from nonusers with respect to age, sex, pay status, and treatment with surgery and tended to differ on treatment with chemotherapy. The univariate logistic models indicated that younger patients (P = .001), women (P = .003), individuals treated with surgery (P = .03) and chemotherapy (P = .12), and indigent patients (P = .038) were more likely to use CAM. Analysis by CAM subtypes revealed that indigent patients were more likely to use psychotherapy (OR, 2.8; 95% CI, 1.2 to 6.6) and vitamins and herbs (OR, 3.2; 95% CI, 1.1 to 9.6) than were patients with partial or full medical coverage. Characteristics of the study participants overall and of CAM users and nonusers are presented in Table 3.
When the five potential predictors were examined in a multivariate logistic regression model, use of CAM was predicted ( 2(4) = 25.5; P < .001) by age (younger), sex (female), pay status (indigent), and surgery (Table 4). Treatment with chemotherapy and pay status did not reach the P < .05 significance level. However, the likelihood ratio test indicated that pay status contributed significantly to the model (2(1) = 5.1; P = .03) and was retained.
Younger patients were 2.1 times (95% CI, 1.2 to 3.6) more likely than older patients and women were 1.8 times (95% CI, 1.02 to 3.1) more likely than men to use CAM. Patients who had undergone surgery were 1.7 times (95% CI, 1.0 to 2.9) more likely to use CAM than those who had not. Although not statistically significant, indigent patients were 4.0 times (95% CI, 0.93 to 17.5) more likely to use CAM than patients who were able to partially or fully pay their medical bills. Therefore, the final logistic model with four variables exhibited a satisfactory fit ( 2(7) = 1.6, P = .98) between obtained and expected outcomes.
When spirituality and psychotherapy/support groups were excluded as CAM therapies, preliminary comparisons by
When the nine potential predictors of CAM use were examined in a multivariate logistic regression model, CAM use excluding spirituality and psychotherapy/support groups was predicted (
Reasons and Expectations for CAM Use A total of 266 patients identified a CAM approach that they used most often and responded to a series of questions about their reasons for using the therapy. Patients reported the most common reason for using CAM was a desire to feel hopeful (73.0%). They also used CAM because they believed these approaches were nontoxic (48.9%) and wanted more control in the decisions about their medical care (43.8%). Patients with distant disease or whose disease could not be staged were more likely to use CAM because their disease was incurable. Specifically, patients who were diagnosed with distant disease at admission were 11.6 times (95% CI, 1.5 to 92.8) more likely to use CAM because their condition was incurable than patients with local disease and 4.2 times (95% CI, 1.3 to 13.7) more likely than patients with regional disease. Furthermore, patients whose disease could not be staged at admission were 14.2 times (95% CI, 1.7 to 118.1) and 5.1 times (95% CI, 1.5 to 18.0) more likely to use CAM because their condition was incurable than patients with local and regional diseases, respectively. Most patients expected CAM to improve their quality of life (76.7%), boost their immune system (71.1%), prolong life (62.5%), or relieve symptoms (44.0%). However, approximately one third of patients (37.5%) expected CAM therapies to cure their disease. Expectations of patients varied according to their stage of disease at admission. Patients with no evidence of disease at admission were 3.1 times (95% CI, 1.3 to 6.9) more likely to expect CAM to relieve their symptoms than those with distant disease. Furthermore, patients whose disease was unstaged at admission, indicating uncertainty about their disease, were 5.6 times (95% CI, 2.3 to 14.0) more likely than those with distant disease and 2.6 times (95% CI, 1.1 to 6.4) more likely than those with regional disease to expect symptom relief with CAM.
Interest in CAM Information and Research
In this survey of 453 outpatients at The University of Texas M.D. Anderson Cancer Center, use of multiple CAM therapies with conventional treatment was widespread, disclosure of CAM use to physicians was low, and the desire for information about CAM was high. This study is the first to assess the prevalence of use in the 1990s at a comprehensive cancer center in the United States and exceeds previous estimates from general populations3,4,25 and cancer populations in the United States.9-11,26-28 Among almost all of the patients who had heard of CAM, the use of at least one CAM modality was 83% or 69% after spirituality and psychotherapy/support groups were excluded. The most popular CAM therapies were spiritual practices, vitamins and herbs, movement and physical therapies, and mind/body approaches. One might conclude that this sample is biased and overestimates CAM use because individuals who may be more inclined to use CAM therapies were more likely to participate (ie, younger patients, women with breast cancer, and patients of higher socioeconomic status). With few exceptions,11,29-31 the literature indicates greater CAM use among younger patients.1,9,28,32-39 However, the effect of sex on CAM use is mixed, with no association29,30,36,39-42 or greater use by women.10,26,37-39 Individuals with higher incomes and who are employed34 or in professional roles37 are more likely to use CAM, with few exceptions.32,36 Although several studies report no relationship between CAM use and disease site,39,41,43 users tend to be patients with lymphoma37 or cancer of the brain or CNS.10,34 Nevertheless, if we conservatively measured CAM use in this study by classifying all nonparticipants as nonusers, the overall prevalence of CAM use would be 44.4% (34.9% after spirituality and psychotherapy/support groups are excluded). This estimate is higher than any survey of cancer patients in the United States reported to date, with the exception of a recent multiethnic, population-based survey that reported that 50% of breast cancer patients in San Francisco use some form of CAM.44 Use of CAM was high in all patient subgroups, but multivariate analysis confirmed that younger patients, women, indigent patients, and individuals treated with surgery were more likely to use CAM. After spirituality and psychotherapy/support groups were excluded, CAM use was predicted by sex (female), but predictors shifted to include education and chemotherapy. Indigent patients were more likely to use herbs and psychotherapy, which may explain in part the change in predictors. Patients who were receiving chemotherapy might have had more advanced disease or been receiving treatment longer and thus had more time to explore options other than spirituality and more conventional psychotherapy/support groups. In support of other studies, however, we found no association between CAM use and marital status,11,30,32,33,37 religious affiliation,26,30,32,33,40,43 ethnicity,11,37,43 disease stage,11,33,36,39 or disease site.39,41,43 CAM use was not associated with the number of primary tumors or metastatic lesions; however, few patients had more than one primary tumor, and approximately 40% had metastatic disease. Our study confirms that the stereotype that terminally ill, desperate, uneducated patients use CAM is inaccurate.11,32 After spiritual approaches, vitamins and herbs were the most frequently used CAM therapies. Although most participants in this study (96%) reported no ill effects with CAM, the potential for harmful drug-herb-vitamin interactions exists45,46 and indicates a need for greater physician communication and more reliable information for patients. Herbs or vitamins can mask or distort18,47 the effects of conventional treatment; however, concurrent use of antioxidants may enhance standard chemotherapy or reduce side effects, depending on the agent and antioxidant combination.48-50 In the absence of definitive evidence, the issue remains controversial. Few patients abandon conventional care,8 and 60% to 80% combine CAM with conventional treatment.10,15,30,32,34,35,38,40,43,51-53 In this study, 72% of patients used two or more, 49% three or more, and 15% seven or more CAM approaches (excluding spirituality and psychotherapy/support groups). The high prevalence of multiple therapy use across the disease continuum suggests that CAM represents an invisible phenomena in mainstream medicine.3 This phenomena could challenge researchers who wish to investigate a single CAM modality. However, this phenomena may be affecting evaluations of conventional therapies, since two thirds of vitamin and herb users also were receiving chemotherapy, radiotherapy, and surgery. Documentation of CAM use should become part of routine assessment for all cancer patients, particularly for patients participating in clinical trials. If physicians are aware that patients are combining these agents with conventional treatment, they can assist them to make more informed choices and monitor them for possible drug-herb-vitamin interactions.54-56 Physicians who are willing to communicate openly and in a nonjudgmental style about CAM may avoid disrupting the patient-provider relationship and possibly encourage compliance with conventional treatment.57 Most patients used CAM to feel more hopeful. Although reasons for hope are not well measured nor the term well-defined,58 hope may be the single greatest reason for using CAM therapies. One third of the outpatients expected CAM to cure their disease, which confirms other studies.10,11,35,37,43,51,59 Stage of disease, although not a predictor of CAM use, influenced patients’ reasons and expectations for using CAM. Patients who had advanced disease were more likely to use CAM because their disease was incurable than those with regional or local disease, but they were less likely to expect symptom relief from alternatives than patients with no evidence of disease or unstaged disease. Patients with regional disease expected symptom relief from CAM more than those whose disease was unstaged. Although we did not assess personality characteristics or satisfaction with conventional care, the literature indicates that patients who use CAM are more optimistic,26 less fatalistic,33 believe stress and cancer are associated,33 and feel they have personal control over their situation.37,38 However, greater anxiety, depression, fear of recurrence,9,33,37 and lower quality of life also have been associated with CAM use.9,11,34 Several studies report that CAM users have less faith in physicians, feel abandoned by their physicians,11,33 and are less satisfied with conventional treatment.11,36 For example, melanoma patients in Austria who used CAM had as much faith in conventional medicine as nonusers but experienced less emotional support from physicians and wanted more supportive interactions.29 In contrast, satisfaction among CAM users in London was lower, largely because of treatment-associated side effects and no hope of a cure.37 Patients who were sicker34 and experiencing more symptoms9 and side effects from chemotherapy,33 particularly nausea,31 were more likely to use CAM. Performance status,15,34,39 physical symptoms,26 and dissatisfaction with conventional care33,38 were not predictors of use in other populations of cancer patients. Several limitations of this study must be acknowledged. First, the sample was restricted to English-speaking outpatients attending M.D. Anderson Cancer Center. These patients may not be broadly representative of cancer patients in the United States. For instance, nearly 70% had received college or postgraduate training. The study also predominantly consisted of white subjects and therefore may not be representative of cancer patients in general. Third, a large proportion of the eligible patients declined to participate in the study. The participants were more likely to be breast cancer patients, younger, and partially or fully covered by medical insurance. As discussed previously, the prevalence of CAM use remained high even when nonparticipants were classified as CAM nonusers. Finally, although no adjustments were made for multiple testing in the univariate models, these exploratory tests were performed only to identify variables to include in the multivariate model, not for definitive conclusions about CAM use. The P values as stated may be used to identify the relative significance levels between the variables tested, but all conclusions on the predictors of use are based on the multivariate analyses. Future studies should be conducted to confirm the results of this study. Unfortunately, the inconsistency in measures of CAM7 and differing patient populations and methodologic approaches (ie, interviews, mailed surveys) limit the generalizability of studies investigating CAM use. To our knowledge, this survey is the first to be conducted across eight major treatment clinics in a comprehensive cancer center in the 1990s. CAM use, including the more conservative measure, indicates that interest in and use of CAM are more widespread than anticipated. Three quarters of these patients expressed interest in learning more about CAM, primarily from their physicians, but most of the patients who used CAM did not feel they could discuss this topic with their physician. Patients want to maximize their chances for survival. Patients with advanced disease turn to CAM for hope after conventional treatment fails34,40; others seek to control or cure the disease and extend survival34,41,59 or improve their quality of life and manage symptoms.34,40,41,59 Parents of children with cancer want to try everything possible after a relapse and seek gentler treatments; approximately one third use herbal teas and extracts, vitamins, and relaxation.43 Similar reports come from parents who turn to vitamins and faith for cures because they perceive no other options for their children.53,60 Alternative therapies have experienced a revival over the past decade, fueled in part by the public’s desire to participate in their own health care and a perception that the medical profession has failed to find a cure for cancer, despite almost three decades of war on cancer.61 This study indicates that patient-provider communication and patient education about CAM should be improved. Furthermore, expanded research initiatives are needed to determine the safety and efficacy of drug and herb or vitamin interactions. Whether we call these approaches medicines, alternatives, unconventional or complementary approaches, or natural herbal remedies, interest in them is here to stay.62 Therefore, the oncology community must be willing to communicate with patients about CAM and inform them about possible contraindications or benefits, integrate CAM approaches that are beneficial or harmless,63 and participate in rigorous research to answer questions of safety and efficacy.
For each therapy listed below, answer the following questions by bubbling in Y for "yes" or N for "no." If you have heard of the therapy, answer the questions about that therapy. If you have not heard of the therapy, bubble N for "no" under "heard of Therapy," indicate if you want to learn about it, and go to the next therapy. 
NOTE. The full questionnaire is available from the authors.
Supported by National Institutes of Health grant no. 5 U24 CA66826-03 through the National Center for Complementary/Alternative Medicine and the National Cancer Institute, Bethesda, MD. We thank Sarah Taylor for providing patient data maintained by Department of Medical Informatics, The University of Texas M.D. Anderson Cancer Center, Houston, TX.
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Copyright © 2000 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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