1 School of Nursing, University of Manchester, Manchester, UK; 2 Institut Català Oncologia ICO, Barcelona, Spain; 3 Faculty of Social Welfare and Health Studies, University of Haifa, Haifa, Israel; 4 Gazi University Hospital, Ankara, Turkey; 5 Department of Nursing and Midwifery, University of Stirling, Stirling, UK; 6 Greek Oncology Nursing Society and Ag. Anargiri Hospital, Athens, Greece; 7 Zurich University Hospital, Poliklinik Onkologie, Zurich, Switzerland; 8 Sahlgrenska University Hospital, Gothenburg, Sweden; 9 Università degli Studi di Milano-Istituto Nazionale Tumori, Milan, Italy; 10 Masaryk Memorial Cancer Institute, Brno, Czech Republic; 11 Oncology Department, Aarhus University Hospital, Aarhus, Denmark; 12 Department of Education, Institute for Oncology and Radiology, Belgrade, Serbia and Montenegro; 13 Belgian Society of Oncology Nursing, Brussels, Belgium; 14 Department of Oncology, Lanspitali, Reykjavik, Iceland; 15 Department of Oncology, City Hospital, Nottingham, UK; 16 School of Health Sciences, Koc University, Istanbul, Turkey; 17 Greek Oncology Nursing Society and Department of Nursing, University of Athens, Athens, Greece
* Correspondence to: Dr A. Molassiotis, University of Manchester, School of Nursing, Coupland III, Coupland Street, Manchester M13 9PL, UK. Tel: +44-161-275-5337; Fax: +44-161-275-7566; Email: alex.molassiotis{at}manchester.ac.uk
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Abstract |
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Methods: A descriptive survey design was developed. Fourteen countries participated in the study and data was collected through a descriptive questionnaire from 956 patients.
Results: Data suggest that CAM is popular among cancer patients with 35.9% using some form of CAM (range among countries 14.8% to 73.1%). A heterogeneous group of 58 therapies were identified as being used. Herbal medicines and remedies were the most commonly used CAM therapies, together with homeopathy, vitamins/minerals, medicinal teas, spiritual therapies and relaxation techniques. Herbal medicine use tripled from use before diagnosis to use since diagnosis with cancer. Multivariate analysis suggested that the profile of the CAM user was that of younger people, female and with higher educational level. The source of information was mainly from friends/family and the media, while physicians and nurses played a small part in providing CAM-related information. The majority used CAM to increase the body's ability to fight cancer or improve physical and emotional well-being, and many seemed to have benefited from using CAM (even though the benefits were not necessarily related to the initial reason for using CAM). Some 4.4% of patients, however, reported side-effects, mostly transient.
Conclusions: It is imperative that health professionals explore the use of CAM with their cancer patients, educate them about potentially beneficial therapies in light of the limited available evidence of effectiveness, and work towards an integrated model of health-care provision.
Key words: alternative medicine, complementary medicine, Europe, herbs, homeopathy, spiritual healing, vitamins
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Introduction |
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A survey conducted in 33 countries, yielding a meagre 83 responses mainly from oncologists, indicated the existence of a large and heterogeneous group of CAM therapies or remedies used to treat cancer in both developed and developing countries [4]. A literature review suggested that the use of CAM among cancer patients is common, with a prevalence rate across studies of 31.4% (range 7% to 64%) [3
]. The latter review included 26 surveys from 13 countries carried out from 1977 to January 1998. However, more recent studies suggest that the use of CAM is considerably higher, with some studies reporting rates of 70.2% in a sample of 356 colon, breast and prostate cancer patients [5
], and 83.3% in an outpatient sample of 453 patients [6
]. Depending on the instrument used to collect the data, the particular population under study, the sample size and the CAM definition used, studies report rates from 37% to 87% [7
11
]. In paediatric patients rates are equally high, ranging from 32.7% in the UK [12
] to 84% in the USA [13
].
The most popular therapies seem to be dietary treatments, herbalism, homeopathy, hypnotherapy and imagery/visualisation [2]. Spiritual therapies, prayer as a therapy, massage, shark cartilage, green tea, support groups and non-traditional diets are also commonly reported in the literature [6
, 9
, 11
, 14
, 15
]. Improvements in physical and psychosocial well-being and increasing hope are the main reasons cancer patients turn to CAM [11
], although dissatisfaction with some aspects of conventional health care, poor doctorpatient relationship, accessibility, perceived effectiveness and desperation may also be key motivating factors [16
].
CAM includes a wide range of therapies. The National Center for Complementary and Alternative Medicine in the USA classifies CAM therapies into five categories [17]:
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Patients and methods |
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Data were collected in the outpatient clinics of a number of hospitals over several random days. On the selected days, all patients attending a given clinic were approached for possible inclusion in the study. In most countries data were collected from more than one hospital, and in five countries there were hospitals included from large cities as well as rural units. Both metastatic and non-metastatic cancer patients were included from cancer centres, oncology units of general hospitals, day units, radiotherapy units and hospices.
All participating patients received information about the study and in most countries those volunteering to participate signed a consent form. However, in a small number of countries (i.e. England) a written consent form was not necessary, and completing the questionnaire implied that patients volunteered for the study. Patients were included if they met the following inclusion criteria: they were adult patients of either gender with a diagnosis of cancer; aware of their diagnosis; able to understand the questions; free from any condition that would make completing the questionnaire inappropriate or overburdening for the patients; and they were willing to participate in the study.
In several countries, especially the Mediterranean and Eastern European ones, data collection proved to be difficult, as a substantial number of patients did not meet one of the inclusion criteria, namely that of being aware of their diagnosis.
Procedures
The questionnaire was anonymous and was handed out to the patients after they received information about the study, agreed to participate and signed the consent form. Patients completed the questionnaire while they were waiting at the outpatient clinic to be seen by their physician or during therapy. On completion, patients either put the questionnaire in a box or handed it to the local researcher. Owing to the multinational nature of the study, it was not possible to assess the number or characteristics of those declining to participate.
The questionnaire
The questionnaire used was based on the one developed by Swisher et al. [11]. However, the questionnaire was modified for the purposes of the present study and some new items were added (for example, personal spending on CAM and frequency of CAM use) and some others were modified to reflect European culture (for example, items on ethnic background and financial status). There were 27 items in total. These included demographic data (age, gender, occupation, education, household income, marital status, number of people living in the household and ethnicity), clinical data (site of primary cancer, standard treatments received previously and current standard treatment) and questions about CAM use.
If patients reported no past or current use of CAM after completing the sociodemographic and clinical section of the questionnaire, they were asked to choose an answer from a list of possible reasons for not using CAM. After that, patients were thanked for their contribution and asked to stop completing the questionnaire at that stage. If patients reported past or current use of CAM, they were asked to continue. The rest of the questions asked were:
Data analysis
Data were analysed using the Statistical Package for Social Sciences (SPSS) programme. Descriptive statistics were calculated with all variables to summarise the data. Differences in sociodemographic characteristics between CAM users and non-users were assessed using the 2-test. Spearman correlation coefficients were also calculated between CAM use and other variables of interest. Finally, multivariate analysis was used to assess which variables predicted CAM use.
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Results |
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The five most frequently used broad categories of therapies were similar across most countries. Herbs were the most commonly used CAM therapy in 13 out of 14 countries and they were the number one CAM therapy in nine countries (Turkey, Israel, Serbia, Czech Republic, Denmark, Italy, Switzerland, Spain and Greece) and in the top five in all countries but Sweden. Homeopathy was the most commonly used CAM therapy in Belgium and in the top five in six other countries (Turkey, Czech Republic, Sweden, Italy, Spain and Greece). Medicinal teas were also in the list of the five most frequently used CAM therapies (seven countries), as were vitamins/minerals (nine countries). Most herbs were specific to each country (i.e. mistletoe in Switzerland, olive leaf paste in Greece, nettle leaves/tea in Turkey, aloe vera in Serbia and Spain or Ovosan in the Czech Republic). Israel, Denmark, Italy, Spain, Greece and Iceland featured strongly in relation to spiritual therapies.
The types of herbs or biological ingestibles used by participants were also assessed, as we asked participants to write down the names of herbs/remedies used. Herbs and other biological ingestibles used included green tea, essiac tincture, Chinese herbs, sage tablets, Echinacea, cod liver oil, fresh juice and vegetables, vitamin E, glucosamine, chamomile, peppermint, selenium, mistletoe/Iscador, yeast extract, multivitamins, Ayurveda herbs, vitamin C, soya drinks, dry thyme, dry nettle, nettle tea, nettle or nettle seeds mixed with honey, ginseng, mulberry molasses, shark cartilage, fish oil, gingko biloba, milk thistle, minerals (i.e. Zn, Ca, Mg), aloe vera (orally and externally used), papaya tea, beet and carrot juice, paste from olive leaves, a mixture of aloehoneyrhaki and wine, and angelica herb. Most herbs were used to treat the cancer, although no participant specified for which specific condition they were using which method.
Patients tended to be satisfied with the use of CAM and they also felt the particular therapy used was effective. The mean satisfaction score was 5.27 (SD 1.52), where a score of 7 indicated the most satisfied. Similarly, the mean score for perceived effectiveness was 5.04 (SD 1.52).
Frequency of use
Thirty-three different types of CAM practitioners were consulted. Seven patients (6.3%) received CAM therapy through their general practitioner/family doctor. Most patients who were visiting a CAM practitioner (n=111) did so less than once a month (34.2%), once a week (24.3%) or once a month (22.5%). Some 8.1% of patients visited a CAM practitioner once a month and 8.1% of patients visited a CAM practitioner 23 times a week. Furthermore, 2.7% visited a practitioner almost daily.
Reasons for using CAM and perceived benefits from its use
Most patients were using CAM as they wanted to increase their body's ability to fight the disease (50.7%), improve physical well-being (40.6%) or improve emotional well-being (35.2%) (Table 5). However, there were some differences in the reasons for using CAM therapies and the experienced benefit from them. In more detail, although the primary reason stated for using CAM was to increase the ability to fight the cancer, only 22.4% found CAM of benefit (P <0.001). Additionally, it is interesting to note that 42.5% found CAM to be helpful in improving emotional well-being, although this was only identified as a reason for use in 35.3% of the sample (P <0.01). Only 31 patients (3.2%) found the CAM therapy/therapies they used were not of benefit at all.
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Side-effects
Fourteen patients (4.4%) reported side-effects from the CAM therapy they had used. Most seemed to be transient side-effects and they were all related to ingesting herbs or minerals. Responses were obtained from seven countries. These side-effects included stomach aches (one incident with thyme and nettle tea, one with vitamin C, and one with aloe); gastric upset and nausea from using nettle tea (one report); itching [one incident with nettle leaves, one with selenium tablets and one with Iscador (mistletoe)]; headaches and migraine (one incident, unspecified herbs); diarrhoea (one incident, unspecified herbs); and poor renal status/accumulation of body acid (one incident with vitamin C).
Multivariate analysis
Spearman correlation coefficients showed that the use of CAM was associated with younger age (rs=0.18; P <0.001), female gender (rs=0.14; P <0.001), higher education level (rs=0.15; P <0.001), higher annual income (rs=0.08; P=0.025) and previous standard treatment (rs=0.12; P <0.001), although these correlations were weak. These were also the variables that differed significantly between the users and non-users of CAM (2-tests). Additionally, occupation was also different between users and non-users (P=0.008). A multivariate model of sociodemographic and clinical characteristics showed that three variables were the strongest predictors of CAM use: younger age, female gender and higher educational level (P <0.001). However, the model could only explain 26% of the variance in the use of CAM.
Why patients do not use CAM
Patients who were not using CAM were asked to note why they did not do so. The majority (n=236; 43.4%) reported that they were happy with the conventional treatment they received/were receiving. Also, 34.7% (n=189) reported that they never thought of CAM and 15.1% (n=82) that they did not believe in CAM. Other reasons included discouragement from family (n=12; 2.2%), lack of information about CAM (n=11; 2%), and inability to pay for CAM (n=9; 1.7%). Five patients (0.9%) noted that they were interested in CAM but they had not decided to use any as yet.
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Discussion |
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More than one-third (35.9%) of the cancer patients reported using some form of CAM, with little variation across countries. This is an increase of the average mean CAM use from that reported in a review of 29 studies covering 20 years [3]. Similar to the study by Ernst and Cassileth [3
], there was great variability in the use of CAM, and this may partly be the result of the patient's understanding of what CAM is. A standardised protocol was used in the current study to minimise such biases, and the definition used was as broad and inclusive as possible. The variability probably also reflects adjunctive use of CAM, as the sample was derived exclusively from health-care settings.
Nevertheless, CAM use is considerably lower in the present study than surveys reporting results from US samples. US studies demonstrate a much higher use of CAM, which is often well above 40% [6, 8
, 9
, 15
]. This could indicate that the concept of a more holistic approach to medicine or the use of an integrated model of health-care provision is lagging in Europe compared with the USA. North Americans may also be using CAM more frequently due to the wider influence that ethnic groups may have had on Western (scientific) medical philosophy, and the realisation that some of the CAM therapies may be beneficial to patients and possibly cost-effective. Furthermore, Kessler et al. [18
] also suggest that the trend in the use of CAM in the USA may be a result of a secular trend that began about half a century ago, which nevertheless highlights the increasing patient demand for such therapies. However, the limited available data on the effectiveness of various CAM therapies also highlights the necessity to be selective and careful (but open minded) about CAM therapies.
The country with the highest CAM use was Italy, but as the source of data was from a palliative care unit these results may not be accurate. An observation of the study was that participants from palliative care facilities tended to use CAM more often, but the mixed settings in most of the countries participating in the study did not allow us to validate this observation. Furthermore, another observation was that CAM use was higher in cities, but when samples from rural hospitals within the same country were added, it decreased the overall number of users. This was especially true in Greece and Spain, where such data were available. Hence, use of CAM therapies may also be related to the availability of such therapies in a given geographical setting. The lowest frequency of CAM use was observed in Greece, and this may reflect the lack of availability of many CAM therapies, high compliance with conventional medical treatments, cultural norms or concealing use of CAM in order to avoid any conflict of opinion with the health-care team. Indeed, before completing the study questionnaire, many participants from a number of countries in the study did mention that they did not want their health-care team to know about their use of CAM.
A large number (n=58) of heterogeneous CAM therapies was reported. Confirming earlier reports, herbals and medicinal teas, vitamins and minerals, spiritual therapies, homeopathy, and relaxation techniques were the CAM therapies used more often in this current sample [711
]. These did not differ substantially among all the countries involved in the study. Perhaps reflecting cultural preferences, availability and national legislation from country to country, differences were observed in the less frequently used CAM therapies. Based on the CAM classification by the National Center for Complementary and Alternative Medicine [17
], most patients were using biologically based therapies. This highlights the attractiveness for patients of natural therapies and remedies, but also suggests that patients may be at risk of side-effects or, as most patients were currently receiving treatment, interactions with conventional medicines. Several good reviews of such side-effects have been presented in the literature (e.g. Niggemann and Gruber [19
]). The role of CAM in affecting (positively or negatively) the outcomes of pharmaceutical clinical trials in cancer care is also an issue that needs attention, as many patients involved in trials will also be using CAM therapies.
Patients typically used more than one CAM therapy together. This fact alone makes research into the effectiveness of CAM using traditional trial designs complicated. It was also interesting to see that only a small number of patients used support groups. This was 0.3% before the diagnosis of cancer (reflecting presence of other chronic conditions), increasing to 1.8% at some point since the diagnosis of cancer and only 1.4% using support groups currently. This is considerably lower than rates reported in past psychosocial literature [20, 21
], perhaps highlighting the lack of availability of support groups in many countries in Europe. However, past research on support groups comes mainly from America, with data commonly collected from breast cancer patients and specialist clinics, so the higher rates reported may not be generalisable to all cancer patients. Further, as can be seen in Table 3, the overall use of energy therapies (often used for wellness rather than specific illnesses) and manipulative methods were decreased after the diagnosis of cancer (with the exception of electromagnetic therapy and massage).
Herbal medicines were by far the most commonly used therapy, escalating in use from 5.3% before the diagnosis of cancer to 13.9% (an almost three-fold increase) after the diagnosis of cancer. A wide range of herbs were recorded as being used. These differed from country to country, probably based on specific ethnopharmacological information and tradition, as well as availability. For example, among others, Turkey reported most commonly the use of nettle leaves/teas, as well as thyme, often mixed with other compounds; Scotland reported more often the use of green tea; Switzerland used mistletoe more often (a particularly popular herb in German-speaking countries); the Czech Republic used Ovosan (a locally produced tablet combining a number of herbs), selenium, ginseng, gingko biloba and Echinacea; Sweden reported the use of blood salts and ginseng; Serbia and Spain reported more often the use of aloe vera; Greece reported the use of a paste made from olive leaves; Iceland reported the use of lupine extracts (angelica) and green tea; and Israel and England reported the use of multivitamins.
It was interesting to see the wide variation in the prevalence rates of CAM use among different diagnostic groups. Despite suggestions from the literature that breast cancer patients are more likely to use CAM compared with other cancer patients [22], the present study showed that pancreatic, liver, bone and brain cancer patients used CAM therapies significantly more often than any other cancer patient group. All four of these diagnostic categories are characterised by poor prognosis and a rapid physical decline, often with metastasis present, and such patients may have little hope from conventional treatments, turning to CAM as an additional intervention to improve their lives. The role of CAM not only in increasing hope and optimism, but also in improving quality of life and managing symptoms, especially in terminal illness, may be important, but relevant data in cancer patients is almost non-existent to date. However, some of the results in this subgroup analysis should be viewed with caution, as only a small number of patients participated from some of the diagnostic categories. Also, a longitudinal design could have given more accurate information about variation of CAM use along the patient's disease experience.
Patients seem to be satisfied with the use of CAM, even if they do not see any obvious benefit from it. A wide range of reasons contribute to the use of CAM, and perhaps the concept of hope is fundamental in each one of these reasons. More than two-thirds of the patients used CAM therapies to directly fight the cancer or to increase the body's ability to fight cancer, but eventually they found little benefit for this. However, those who used CAM to improve physical and emotional well-being seemed to have benefited from CAM. These findings coincide with findings from the USA [11]. It is interesting to see that <1% of the patients used CAM following the recommendation of their physician, perhaps reflecting the disapproval of CAM therapies by the medical community or the lack of information to the medical community about available and effective CAM therapies. Examples of such information include the consistently positive results with acupuncture in the management of chemotherapy-related nausea and vomiting [23
]; the positive effects of self-hypnosis, massage or acupuncture in pain relief in cancer patients [24
]; the relief of dyspnoea with acupuncture, acupressure or relaxation/breathing techniques [24
]; the positive short-term benefits of massage and aromatherapy massage on psychological well-being [25
]; and the promising results from the use of mistletoe in relation to survival, management of side-effects or quality of life in cancer patients [26
]. Also, <4% used CAM to directly fight the disease (i.e. as an alternative cancer treatment) and the overwhelming majority used CAM to complement their cancer treatment or help them cope with the treatment and/or its side-effects. As many of the therapies used are complementary in nature (such as aromatherapy, massage, relaxation, reflexology and others), we may not need to prove their effectiveness before using them, as patients are demanding such therapies, they are low-risk therapies and patients feel good after their use. Such therapies may have a great role to play, especially in the palliative care setting, where the goal is not cure but rather improvement in quality of life. Patient satisfaction can be an appropriate end point outcome for evaluation rather than clinical outcome studies in this setting.
A wide variety of sources of information were used before patients selected a given therapy. Friends and family or word of mouth seemed to be the most important sources of information. This may be problematic, as what is effective for one patient may not be for another, even with the same symptoms. Also, the media was shown to be a common source of information, and this may again be problematic, as the media often sensationalises patient stories without balancing the information presented. The role of physicians as sources of information was quite low, with only 18.6% actually providing information to patients. This number is even lower among nurses: only 3% of nurses were identified as the main source of information for patients. Health professionals need to be able to provide information about CAM to their patients, although the knowledge deficit is acknowledged. The Internet is another commonly used source of information, but the commercial nature of many relevant websites (especially in relation to herbs) and the lack of quality assessment of the information posted on the web may be sources of misinformation [27].
Findings should be evaluated in light of the limitations of the study. The European-wide nature of the study was difficult to conduct, and it was difficult to maintain consistency, because of its international breadth and specific requests from various ethics committees or hospital boards. As we did not have access to medical records, we could not ascertain whether there was metastatic disease or not and other, more sensitive clinical data. There is also an overlap between the users of CAM since diagnosis and currently. Based on the selected design of the study, made simple and anonymous to fulfil recruitment criteria in all the countries involved, it was difficult to track patients who refused participation (albeit recruitment rates of >90% were achieved in the majority of the cases, based on individual researchers' comments). Finally, as the samples were taken from different settings, patterns of use may reflect different rates because of the setting rather than the countries concerned.
Irrespective of what health professionals believe about CAM and how dismissive of CAM they may be, it is evident that patients are using, and will continue to use, CAM therapies. Hence, from a professional point of view, health-care staff need to be aware of such use of CAM and to be able to educate patients appropriately. This will probably necessitate the rethinking of the provision of medical and health-care education, broaden our understanding of the concept of medicine and help us work towards integrating into mainstream health-care services those CAM therapies for which evidence of effectiveness exists. This debate has already been discussed elsewhere (i.e. Owen et al. [28]). At the same time, there will be a need for considerable increase in the funding for CAM research. Currently only the National Center for Complementary and Alternative Medicine, National Institutes of Health in the USA provides substantial funds for such research, and other organisations and countries would need to follow their example. In the UK, research funding for CAM has increased over the years but, until recently, this was still only
0.31% of all funding available for medical research, suggesting that funding is low [29
]. The need to increase the evidence base of CAM therapies, using methodologies that are appropriate and sensitive to CAM, cannot be overemphasised. This is also important from an economic point of view, as the use of CAM is a multibillion Euro business, and as shown in this study, some patients pay large sums out of their pockets to receive such interventions. In the USA, where such data are available, the use of CAM is conservatively estimated to cost patients US$27 billion (for the year 1997) [30
]. In Europe it is the second biggest growth industry [31
]. Finally, appropriate legislation and regulation of CAM therapies in Europe is also necessary. While many countries have developed their own regulation and legislation [32
], there are wide variations in such laws across Europe. Since it would appear that CAM is here to stay, the European Community needs to consider broader policies, common laws and a rationalisation of the available legislation.
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Acknowledgements |
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Received for publication June 17, 2004. Revision received November 5, 2004. Accepted for publication November 15, 2004.
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