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Expected and perceived efficacy of complementary and alternative medicine: A comparison views of patients with cancer and oncologists
Complementary Therapies in Medicine 28 (2016) 29–36
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Complementary Therapies in Medicine journal homepage: www.elsevierhealth.com/journals/ctim
Expected and perceived efficacy of complementary and alternative medicine: A comparison views of patients with cancer and oncologists Sang Hyuck Kim (MD) a , Dong Wook Shin (MD, DrPH, MBA) a,b,∗∗ , You-Seon Nam (MD) c , So Young Kim (MD, PhD) d,e , Hyung-kook Yang (MD) d , Be Long Cho (MD, MPH, PhD) a,b,f,g , Keeho Park (MD, MPH, PhD) h , Heui-Sug Jo (MD, PhD) i , Chang-Yeol Yim (MD, PhD) j , Sin Kam (MD, PhD) k , Jong-Hyock Park (MD, MPH, PhD) d,l,m,∗ a
Department of Family Medicine & Cancer Survivorship Clinic, Seoul National University Hospital, Seoul, Republic of Korea Laboratory of Health Promotion and Health Behavior, Biomedical Research Institute, Seoul National University Hospital, Republic of Korea c Department of Family Medicine, Seoul National University College of Medicine, Seoul, Republic of Korea d National Cancer Control Institute, National Cancer Center, Goyang, Republic of Korea e Regional Cardiocerebrovascular Center, Chungbuk National University Hospital, Cheongju, Republic of Korea f Institute on Aging, Seoul National University College of Medicine, Seoul, Republic of Korea g Advanced Institutes of Convergence Technology, Seoul National University, Suwon, Republic of Korea h Cancer Policy Branch, National Cancer Center, Goyang, Republic of Korea i Department of Health Management and Policy, Kangwon National University School of Medicine, Chuncheon, Republic of Korea j Department of Internal Medicine, Chonbuk National University Medical School, Jeonju, Republic of Korea k Department of Preventative Medicine, School of Medicine, Kyungpook National University, Daegu, Republic of Korea l Department of Health Informatics and Management, College of Medicine, Chungbuk National University, Cheongju, Republic of Korea m Graduate School of Health Science Business Convergence, Chungbuk National University, Cheongju, Republic of Korea b
a r t i c l e
i n f o
Article history: Received 17 March 2016 Received in revised form 15 July 2016 Accepted 29 July 2016 Available online 29 July 2016 Keywords: Complementary and alternative medicine Discrepancy Oncologist Cancer patient Efficacy
a b s t r a c t Background & aims: This study sought to identify discrepancies between the expectations of patients with cancer and oncologists regarding the efficacy of complementary and alternative medicines (CAMs), and to determine how patients evaluate CAM efficacy after its use. Methods: Data from the Cancer Patient Experience Study, a nationwide survey, were used. Seven subdivided efficacy domains were included in the survey. An oncologist-patient matching analysis was done to assess the concordance of CAM efficacies between oncologists and patients with cancer. In addition, the patients’ expectations of CAM efficacies were compared before and after use. Results: Out of 719 participants, 201 patients with cancer (28.0%) reported using CAMs. The patients with cancer generally tended to be more positive about CAM efficacies than the oncologists. The largest discrepancy in efficacy perception was found in the efficacy domain of survival benefit, which included complete disease remission and prolonged survival. Many patients reported that they did not experience the positive efficacy they had anticipated before use. However, a substantial proportion of patients indicated that CAMs were as effective as they had expected, even though there is little evidence supporting the CAM efficacies. Conclusions: There was a marked discrepancy and a lack of concordance in expectations of CAM efficacy between patients with cancer and oncologists. Better communication between the patients and oncologists regarding CAM efficacy would be needed to make the patients to have shared expectations, and to reduce unnecessary CAM use. © 2016 Published by Elsevier Ltd.
1. Introduction ∗ Corresponding author at: College of Medicine/Graduate School of Health Science Business Convergence, Chungbuk National University, Cheongju 28644, Republic of Korea. ∗∗ Corresponding author at: Department of Family Medicine, Seoul National University, College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul 03080, Republic of Korea. E-mail addresses: [email protected] (D.W. Shin), [email protected] (J.-H. Park). http://dx.doi.org/10.1016/j.ctim.2016.07.005 0965-2299/© 2016 Published by Elsevier Ltd.
Currently, the use of complementary and alternative medicines (CAMs) in patients with cancer is widespread and increasing.1–4 Accordingly, an enormous amount of money is being spent in this field.1,2 In a survey conducted in Korea, approximately 78.5% of
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patients with cancer used at least one type of CAM, with a mean monthly cost of $1100 per person.2 However, most clinically implemented CAMs have limited scientific evidence, which is inconclusive to recommend their use.5–7 Even CAMs may induce unwanted negative consequences for conventional cancer treatment, not only directly but also by interfering with the metabolism and the physiological response of conventional treatment.8–10 Therefore, clear communication about CAM use between the patient and their physician is important when deciding on cancer treatment. The use of CAMs is largely driven by expectations of their efficacy by patients with cancer.11,12 Some previous studies revealed that patients with cancer often have much higher expectations of CAM efficacy than physicians.3,13,14 However, these studies did not match the patients with their doctors to assess the concordance of expected CAM efficacies. In addition, experienced efficacy after CAM use are the basis for the decisions of patients with cancer on continued CAM use,15 which can also affect the initiation of CAM usage in other patients with cancer.3,16 Therefore, it is necessary to know how patients evaluate CAM efficacies after their use compared to their initial expectations prior to CAM use. However, to our knowledge, there are no studies comparing the expected efficacies of CAMs with their experienced efficacy after CAM use in patients with cancer. Understanding both the patients’ and physicians’ perspectives on CAMs would help establish better decision making for CAM use. In this study, we compared (1) the expected efficacies of CAMs in patients with cancer and the perceived efficacies of CAMs in their oncologists with a matched patient-physician sample, and (2) the expected and experienced CAM efficacies in patients with cancer before and after use, respectively. 2. Materials and methods 2.1. Study design and subjects This study was conducted as part of the CaPE (Cancer Patient Experience) Study, an annual nationwide survey in Korea, which assesses medical care and treatment options for cancer. This study was supported by the Ministry of Health and Welfare, and conducted by the National Cancer Center. It was approved by the institutional review board of the National Cancer Center (Grant No. 1210150). The survey was conducted in 2012 using oncologist–patient with cancer–caregiver matched triads, to explore the different views of oncologists, cancer patients and family caregivers in medical care and treatment. Trained nurses helped the participants to complete and understand the survey questionnaires. The detailed process for recruiting oncologists, patients with cancer, and their caregiver has been described previously.17 Briefly, a total of 144 board-certified oncologists were recruited from 13 cancer centers. Each oncologist was asked to recruit 6 consecutive patients who were accompanied at the visit by a family caregiver. Among the 144 oncologists, 134 completed the study survey (93.1% participation rate). From the 960 patients, 725 dyads and their caregivers completed the survey (75.5% participation rate). 2.2. Survey questionnaires The CAM questionnaire was administered only to patients and physicians, in order to have matched analyses. The English version of the survey questionnaires is provided as online-only Supplementary material. The patients were first asked whether they had ever used CAMs after their cancer diagnosis for cancer care. If the answer
was ‘Yes. But not now’ or ‘Yes. I am currently using’, they were asked to describe the type of CAM used. We presented 8 CAM categories in the survey questionnaire, which are designated as CAM Therapies by the Office of Cancer Complementary and Alternative Medicine, The National Cancer Institute (NCI)18 : (1) Alternative Medical System (e.g., acupuncture, moxa cautery, cupping therapy, ayurveda, traditional Chinese medicine, homeopathy, naturopathy); (2) Energy/Exercise Therapy (e.g., tai chi, qi gong, yoga); (3) Manipulative and Body-Based Methods (e.g., chiropractic manipulation, massage, osteopathic manipulation); (4) Mind-Body Interventions (e.g., meditation, hypnosis, biofeedback, imagery, relaxation, music therapy, aromatherapy); (5) Spiritual Therapies (e.g., intercessory prayer and spiritual healing); (6) Dietary Therapy (e.g., vegetarian diet, Gerson diet); (7) Nutritional Therapeutics (e.g., vitamin, melatonin, mineral supplement, herb and herbal extract); and (8) Others. Some category modifications were made to take into account the prevalence and general concept of CAMs in Korea. For example, energy and exercise therapy were combined into a single category since Koreans tend not to conceptually distinguish these two examples. Dietary therapy and nutritional therapeutics were separated, as many Koreans do not equate specific dietary therapy and nutritional supplements. The ‘pharmacological and biologic treatments’ NCI category was not included in the response options, since these treatments (e.g., antineoplastions, 714X, low dose naltrexone) are generally not available or practiced in Korea. Since patients could use more than one CAM type, multiple responses were allowed. The patients were asked about their expectations on CAM efficacies before use on the following items: (1) complete remission of disease; (2) life prolongation; (3) pain or symptom relief; (4) regaining physical strength; (5) immune function improvement; (6) psychological and emotional support for the patient; and (7) psychological and emotional support for their family caregivers. Response options were yes or no. Simultaneously, they were also asked whether they experienced CAM efficacy on the same items after CAM use. Finally, the patients were asked if they had discussed about CAM use with doctors. The physicians were asked about their opinions on the general efficacy of CAMs using the same set of questions. Also, they were asked if they had discussed about CAM use with their patients. In addition, the survey collected the respondents’ sociodemographic and medical information. Further, the primary cancer diagnosis using the Surveillance, Epidemiology, and End Results (SEER) stage criteria was retrieved from the hospital information systems of each participating center.
2.3. Statistical analysis A descriptive analysis was performed for the respondents’ baseline characteristics. We compared the proportions of positive responses to the expected efficacy items in both medical oncologists and surgical oncologists. Radiotherapy oncologists were excluded in the analysis due to possible bias by the small sample size of included radiotherapy oncologists (n = 7). The proportion of positive responses to the expected efficacy items from the oncologists and the patients was compared using a chi square test. After matching the patients to their own doctor (multiple patients with cancer could be matched to a single oncologist), a Cohen’s Kappa and the p values from the McNemar test were calculated to assess the concordance of the responses between the oncologist and their own patients. The proportions of positive response to items regarding the expected and experienced CAM efficacies were compared using a McNemar test. All statistical analyses were conducted using STATA software version 14.0 (StataCorp., TX). A p value of less than 0.05 was considered statistically significant.
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Table 1 Respondents’ Characteristics According to the Experience of CAM use (n, %). Ever Useda (n = 201) Mean Age (SD) Sex Male Female
P value†
Never Used (n = 518)
59.4
(12.8)
60.5
(12.8)
0.267
87 114
(43.3) (56.7)
242 276
(46.7) (53.3)
0.407
Educational Status <9 years 9–12 years >12 years Missing
78 66 56 1
(38.8) (32.8) (27.9) (0.5)
265 167 82 4
(51.2) (32.2) (15.8) (0.8)
0.001
Monthly Income (KRW) <2 million ≥2 million Missing
110 88 3
(54.7) (43.8) (1.5)
310 203 5
(59.9) (39.2) (1.0)
0.236
Cancer Type (Primary) Stomach Lung Liver Colon Breast Cervix Others
21 27 14 44 39 12 44
(10.5) (13.4) (7.0) (21.9) (19.4) (6.0) (21.9)
97 70 38 85 63 37 128
(18.7) (13.5) (7.3) (16.4) (12.2) (7.1) (24.7)
0.023
Treatment Situation Under Initial Treatment On Regular Follow-up after Treatment On Regular Follow-up after Cure Under Treatment for Metastasis of recurrence Do Not Know Others (Ex. Treatment for Second Primary Cancer) Missing
76 74 18 29 3 1 0
(37.8) (36.8) (9.0) (14.4) (1.5) (0.5) (0.0)
246 161 21 76 11 2 1
(47.5) (31.1) (4.1) (14.7) (2.1) (0.4) (0.2)
0.047‡
SEER Stage at the Time of Diagnosis In Situ or Local Regional Distant Unknown/Missing
80 75 42 4
(39.8) (37.3) (20.9) (2.0)
210 199 99 10
(40.5) (38.4) (19.1) (1.9)
0.948‡
CAM, complementary and alternative medicine; KRW, Korean Won; SEER, Surveillance, Epidemiology, and End Results Program. a Respondents who were using or previously used CAMs after cancer diagnosis for cancer care were included. † t-test for continuous variables and chi-square test for categorical variables. ‡ Obtained from the Fisher’s exact test.
3. Results 3.1. Patient experiences with CAM use and oncologist characteristics Table 1 provides the baseline patient characteristics. Among the original 725 patients with cancer who participated in the CaPE Study, 719 (99.2%) answered the questionnaire regarding their CAM usage. Among these, 140 patients (19.5%) responded that they were using at least one type of CAM at the time of the survey, and 61 patients (8.5%) reported that they had previously used at least one type of CAM after cancer diagnosis for cancer care but were not currently using it. The majority of the respondents had never used CAMs. Higher educational status, cancer type (e.g. stomach, colon, and less common cancers), and treatment situation were significantly associated with CAM. However, other characteristics including age, sex, monthly income, and SEER stage at the time of diagnosis were not significantly associated with CAM use. Table 2 indicates the patient usage in each CAM category. Among the 201 patients who had used a CAM after their cancer diagnosis, the majority of patients reported they had used nutritional or dietbased therapies. A relatively small proportion of patients had used mind-body interventions, spiritual therapy, or manipulative and body-based methods A total of 134 oncologists participated in the CaPE Study. Their subspecialties included medical oncology (n = 59, 44.0%), surgical oncology (n = 68, 50.7%), and radiotherapy (n = 7, 5.2%). The
Table 2 Categories of CAMs Used By Patients (n, %). Alternative Medical System Energy/Exercise Therapy Manipulative and Body-Based Methods Mind-Body Interventions Spiritual Therapies Dietary Therapy Nutritional Therapeutics Others
45 74 13 26 23 112 126 1a
(22.4) (36.8) (6.5) (12.9) (11.4) (55.7) (62.7) (0.5)
CAM, complementary and alternative medicine. Total number of respondents who used CAMs was 201. a Using electric potential therapy device.
efficacy of CAMs on immune function improvement was significantly different across the oncologists’ subspecialties, with no significant differences in the other expected efficacies (Table 3). 3.2. Patients’ expected efficacy and physician’s perceived efficacy of CAMs: a comparison of the patients’ and oncologists’ views The comparison of efficacies expected by patients with cancer and the oncologists’ perceived efficacies of CAMs are shown in Fig. 1. More than half of the patients expected positive efficacy with CAM use regarding complete remission of their disease, life prolongation, pain or symptom relief, and psychological and emotional support for their family caregivers. Moreover, approximately 80% of patients with cancer expected CAMs to be efficacious in
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Table 3 Oncologists’ Expected Efficacies of CAMs Grouped according to Their Specialties (n, %). Medical Oncologist (n = 59).
Surgical Oncologist (n = 68)
Radiotherapy Oncologist (n = 7)
Yes
Yes
Yes
No
No
P valuea
No
Complete Remission of Disease (n = 134) Life Prolongation (n = 134) Pain or Symptom Relief (n = 134) Regaining physical strength (n = 134) Immune Function Improvement (n = 134)
2 3 35 24 21
(3.4) (5.1) (59.3) (40.7) (35.6)
57 56 24 35 38
(96.6) (94.9) (40.7) (59.3) (64.4)
3 6 50 39 37
(4.4) (8.8) (73.5) (57.4) (54.4)
65 62 18 29 31
(95.6) (91.2) (26.5) (42.6) (45.6)
0 0 4 5 5
(0.0) (0.0) (57.1) (71.4) (71.4)
7 7 3 2 2
(100.0) (100.0) (42.9) (28.6) (28.6)
1.000 0.698 0.208 0.090 0.043
Psychological and Emotional Support For Patient (n = 134) For Family Caregivers (n = 134)
54 48
(91.5) (81.4)
5 11
(8.5) (18.6)
63 58
(92.6) (85.3)
5 10
(7.4) (14.7)
7 7
(100.0) (100.0)
0 0
(0.0) (0.0)
1.000 0.622
CAM; complementary and alternative medicine. a Obtained from the chi-square test or Fisher’s exact test as appropriately.
Fig. 1. Patients’ and Doctors’ Expected CAM Efficacies. All of the 134 doctors responded to the each efficacy category. The total numbers of the cancer patients in each category were different due to different response rates (complete remission of disease, n = 195; life prolongation, n = 194; pain or symptom relief, n = 193; regaining physical strength, n = 195; immune function improvement, n = 196; psychological and emotional support for patient, n = 194; psychological and emotional support for family caregivers, n = 193). All p values from the t-test were below 0.001, except for RPS (p = 0.070) and PESFC (p = 0.001).
regaining physical strength, immune function improvement, and psychological and emotional support for the patient. Unlike the patients’ responses, very few oncologists viewed CAMs as an efficacious treatment for the complete remission of disease (n = 5, 3.7%) and life prolongation (n = 9, 6.7%). Approximately half of the oncologists endorsed CAMs for their positive efficacy in pain or symptom relief, regaining physical strength, and immune function improvement. For these items, patients’ expectation were significantly higher than the perceived efficacy by oncologists, except for pain or symptom relief (p = 0.070). In contrast, the oncologists were highly positive regarding efficacies of CAMs for the psychological and emotional support of the patient, and for the family caregivers. These measures were significantly higher than the measures of patients’ expectations.
We performed a doctor-patient matching analysis to assess the concordance of expected CAM efficacies between the oncologists and patients (Table 4). A total of 134 oncologists were matched to their own patients. Agreement rates for Complete Remission of Disease, life prolongation, relief of pain or symptoms, reinforcement of physical strength, immune function improvement, psychological and emotional support for patients and families were 44.6%, 46.9%, 53.4%, 55.4%, 57.1%, 73.2%, and 66.3%, respectively. No significant concordance was observed between the patients’ expected efficacy and the oncologists’ perceived efficacy. The highest kappa was 0.156 for immune function improvement. P values from the McNemar test were below 0.001 in all efficacies of CAMs except for the relief of pain or symptom (p = 0.011).
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Table 4 Doctor-Patient Matching Analysis about CAMs’ Efficacy (n, %). Doctors’ Expected Efficacy Patients’ Expected Efficacy
Yes
No
Agreement (%)
kappa (SE)a
†
P value
Complete Remission of Disease
Yes No
6 3
(3.1) (1.5)
105 81
(53.8) (41.5)
87
(44.6)
0.016 (0.026)
<0.001
Life Prolongation
Yes No
7 5
(3.6) (2.6)
98 84
(50.5) (43.3)
91
(46.9)
0.010 (0.032)
<0.001
Relief of Pain or Symptoms
Yes No
76 57
(39.4) (29.5)
33 27
(17.1) (14.0)
103
(53.4)
0.019 (0.070)
<0.011
Reinforcement of Physical Strength
Yes No
85 14
(43.6) (7.2)
73 23
(37.4) (11.8)
108
(55.4)
0.099 (0.057)
<0.001
Immune Function Improvement
Yes No
80 15
(40.8) (7.7)
69 32
(35.2) (16.3)
112
(57.1)
0.156 (0.060)
<0.001
Psychological and Emotional Support Yes For Patient No
139 40
(71.6) (20.6)
12 3
(6.2) (1.5)
142
(73.2)
0.013 (0.060)
<0.001
Yes No
112 46
(58.0) (23.8)
19 16
(9.8) (8.3)
128
(66.3)
0.128 (0.067)
<0.001
For Family Caregivers
CAM, complementary and alternative medicine; SE, standard error. The total numbers of the cancer patients in each category were different due to different response rates. 134 oncologists matched to their own patients. a Cohen’s kappa after doctor-patient matching. † Obtained from the McNemar test.
3.3. Expected efficacy and self-reported efficacy after use: patients’ view Fig. 2 shows the comparison of the expected efficacy and the self-reported efficacy after use in patients with cancer. Generally, the proportions of positive CAM efficacies after use were lower than those of the expected efficacies before use. However, a substantial proportion of patients thought that CAMs were effective for the complete remission of diseases (before use: 58.3%; after use: 35.3%; p = 0.001), life prolongation (before use: 55.4%; after use: 33.9%; p = 0.001), and pain or symptom relief (before use: 58.4%; after use: 42.2%; p = 0.001). More than half of the patients reported a positive effect for CAMs on regaining physical strength, immune function improvement, and psychological and emotional support for patients, and for family caregivers.
3.4. Experience of counseling for CAM use One third of cancer patients (n = 71, 35.9%) in the present study had indicated that they did not counsel about CAM use with their doctors. Only 23.9% (n = 32) of oncologists in the present study reported that they had discussed about CAM use with their patients.
4. Discussion To our knowledge, this is the first study which compared expected efficacies of CAMs among cancer patients with those among the oncologists, as well as with self-reported experienced efficacies after use. Our study design employed doctor-patient matching and pre- and post-CAM use matching, which enabled us to explore the difference in viewpoints between the patients and their physicians in a clinical setting as well as the dynamic shift of the patients’ perspective on their perceived efficacy of CAMs. Additional strengths of this study include systematic sampling methods with a high response rate, supporting the generalizability of these results across the Korean population.
4.1. Use of CAMs in Korean cancer patients In this study, approximately 28.0% of patients with cancer reported CAM use. This figure is much lower than those in previous reports on CAM prevalence in Korea.2,13,19,20 This may be due to the differences in CAM definitions. For example, one previous study presented ‘mushroom’ and ‘honey’ as examples of CAMs, while ours did not include such a definition.20 In addition, there may be differences in the response rate, the included cancer centers, and the characteristics of the patients with cancer included in this study. However, the reported prevalence of CAM use in this study is similar to that found in our 2008 survey, which was conducted in 10 cancer centers (the prevalence of CAM use was 25.5%).21 Like many other studies, the most frequently used CAM type was diet-based and included food supplements, such as herbs and herbal extracts.2,15,19 A considerable proportion of respondents used energy/exercise therapy. In this study, a higher educational status, colon or breast cancer diagnosis, and treatment situation (e.g., ‘on regular follow-up after treatment’) were significantly associated with CAM use. A higher educational status has been consistently identified as a factor associated with higher CAM use in patients with cancer.16,22,23 While the reasons for this association are not clear, some studies suggest that the relatively sufficient financial resources enable this population to bear the additional cost of CAMs.20,23 The reason for higher CAM use in patients with colorectal or breast cancer could not be determined by our study design. However, a previous study suggested different patterns of CAM use among patients with different cancer types.20 Additionally, patients who were on regular follow-up after treatment showed higher prevalence of ever CAM use than who were on initial treatment. One possible reason could be that patients who had finished initial treatment felt the urge to do “something” for their health, and seek CAM use. However, further studies are needed to address this question. 4.2. The discrepant view between patients with cancer and oncologists regarding CAM efficacy Consistent with previous studies,3,13,14 this study showed a marked discrepancy between the expectations of patients with
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Fig. 2. Expected and Self-Reported CAM Efficacies in Patients with Cancer. The total numbers of the respondents in each category were different due to different response rates (complete remission of disease, n = 187; life prolongation, n = 186; pain or symptom relief, n = 185; regaining physical strength, n = 190; immune function improvement, n = 190; psychological and emotional support for patient, n = 189; psychological and emotional support for family caregivers, n = 186). All p values from the McNemar test were below 0.001, except for psychological and emotional support for patient (p = 0.028), and psychological and emotional support for family caregivers (p = 0.289).
Table 5 Patients’ Expected Effects of CAMs grouped according to the SEER Stage at the Time of Diagnosis (n, %). In Situ or Local
Regional
Yes
Yes
No
Distant No
Yes
Unknown/Missing No
Yes
P valuea
p for trend
No
Complete Remission of Disease (n = 195) Life Prolongation (n = 194) Pain or Symptom Relief (n = 193) Regaining physical strength (n = 195) Immune Function Improvement (n = 196)
37 32 35 62 56
(48.1) (41.6) (46.1) (80.5) (72.7)
40 45 41 15 21
(51.9) (58.4) (53.9) (19.5) (27.3)
46 45 46 61 59
(63.0) (61.6) (63.9) (84.7) (80.8)
27 28 26 11 14
(37.0) (38.4) (36.1) (15.3) (19.2)
25 25 24 32 30
(61.0) (62.5) (58.5) (76.2) (71.4)
16 15 17 10 12
(39.0) (37.5) (41.5) (23.8) (28.6)
3 3 4 3 4
(75.0) (75.0) (100.0) (75.0) (100.0)
1 1 0 1 0
(25.0) (25.0) (0.0) (25.0) (0.0)
0.147 0.022 0.084 0.523 0.403
0.111 0.014 0.107 0.702 0.925
Psychological and Emotional Support For Patient (n = 194) For Family Caregivers (n = 193)
60 48
(78.9) (63.2)
16 28
(21.1) (36.8)
56 50
(76.7) (69.4)
17 22
(23.3) (30.6)
32 30
(78.0) (73.2)
9 11
(22.0) (26.8)
3 3
(75.0) (75.0)
1 1
(25.0) (25.0)
0.947 0.502
0.867 0.248
SEER, Surveillance, Epidemiology, and End Results Program. The total numbers of the respondents in each category were different due to different response rates. The respondents whose SEER stages were ‘Unknown/Missing’ were excluded for the calculation of the p-values and the p for trend. a Obtained from the chi-square test.
cancer regarding CAM efficacy and the perception of the oncologists. Since patients were generally positive regarding CAM efficacy, it is possible that many patients used a CAM treatment that their own physician did not think was effective. The largest discrepancy was observed within the domain of complete remission of disease or prolonged survival. In particular, patients with more advanced cancer stages were more likely to expect life prolongation (Table 5 p for trend = 0.014). A previous study suggested that patients with cancer believed that CAMs could replace conventional treatment in advanced cancer stages.24 On the other hand, most oncologists were aware that there is currently minimal evidence for improved survival from any CAM therapy.5,7,25 In this study, the oncologists supported the use of CAM as helpful for the patients’ psychological and emotional support. These discrepancies should be addressed
during treatment consultations, regardless of the patients’ actual CAM usage. The lack of concordance revealed by our unique matched analysis suggests that patients and their physicians do not share common views before treatment initiation. Previous studies have suggested that a substantial proportion of patients with cancer do not disclose CAM use to their doctors,26,27 and that oncologists are generally not willing to have conversations about CAMs with their patients.13,26 Similarly, in our study many patients who ever used CAM said that they did not counsel about CAM use with their doctors. Furthermore, only a minority of oncologists in the present study reported that they had discussed about CAM use with their patients. Such a lack of conversation about CAMs may lead to discrepant views between the patients and their physicians, inadequate decision
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making about CAM use, and even harmful effects for the patients. This highlights the need for better communication between the oncologists and their patients regarding the CAM use to provide better guidance for patients. Even if the existing evidences are not enough, oncologists need to discuss with their patients about possible benefits and harms of CAM.
Finally, the present study is a cross-sectional survey, and is susceptible to recall bias. The response about their past thinking could be affected by what occurred after that. A prospective study might be needed to overcome such bias.
4.3. Patients’ perception of actual benefit after CAM use
In conclusion, our study showed a marked discrepancy and a lack of concordance between the expectations of patients with cancer regarding CAM’s efficacy and the perception of the oncologists. In addition, we found that a substantial proportion of patients believed that CAMs were as effective as they had expected. Considering low consultation rate of CAM use, better communication between the patients and oncologists regarding CAM efficacy would be needed to make the patients to have shared expectations, and to reduce unnecessary CAM use.
Many patients with cancer reported that they did not actually experience the positive CAM efficacies they expected before use. This was most evident when the patients expected a physical effect after CAM use, such as complete remission, life prolongation, or pain and symptom relief. However, a substantial proportion of patients indicated that CAMs were as effective as they had expected. Despite the limited scientific evidence of CAMs,5,7–10 there may be some unmet needs contributing to the expected and experienced CAM efficacies in patients with cancer.13 To identify and to fill such needs can improve patients’ quality of life and their satisfaction of cancer treatment. Further studies to investigate on this are needed. Validating the patients’ perception about the experienced efficacy is beyond the scope of our study. Nevertheless, a subjective, positive experience may lead to the continuation of CAM use,15 and even a recommendation of CAM use to other patients.3,16 Therefore, our findings suggest that patients’ beliefs about CAMs are not easily modified by a simple description of CAMs as ineffective. While oncologists need to provide evidence-based information about CAMs, they should not discourage or disapprove CAM use, but rather listen to the patient’s needs, worries, and intents behind CAM use. Otherwise, the discrepancy in the oncologists’ views on CAM efficacy can lead to patients’ concealment of CAM use to their physician. Integrative oncology programs, which have been established in several cancer centers, may provide evidence-based information and support for making appropriate decision regarding CAM use.11 One notable limitation of this study is the discrete categorization of various CAMs. In fact, CAMs in the same category may have different efficacies. Furthermore, many patients with cancer may use various types of CAMs. Therefore, if specific types, rather than categorization of CAMs were used, we may have obtained different results. However, since we used CAM categorization, the general perception about the various CAMs could be evaluated. Second, we presented only “Yes” or “No” as answer choices. More options, such as a Likert-type scale, may enable a more sensitive evaluation of the different expectations between cancer patients and oncologists. Nonetheless, the different expectations about CAM efficacy in the present study are consistent with previous studies.3,13,14 Therefore, the possible limitations of the presented choices might be minimal. Third, as the present study focused on the efficacies of CAM, questionnaires regarding possible harms of CAM were not included in the survey. As expected or experienced harms of CAM can affect initiation or continuation of CAM use, further studies are needed to address this issue. Fourth, we did not take into account the duration of CAM use. The efficacy domains of “Complete remission of disease” and “Life prolongation” need several years for patients with cancer to be able to say conclusively that they are in remission or have had survival benefits. In addition, if patients were using CAMs simultaneously with conventional cancer treatment, it could be very difficult for cancer patients to distinguish the different efficacies of CAMs and conventional cancer treatments. However, the study design of the present study, which dealt with CAM efficacy before and after CAM use, may be enough to identify cancer patients’ positive view regarding CAM efficacy even in the remission of the disease and life prolongation.
5. Conclusion
Conflict of interest statement The authors have no potential conflicts of interest. Acknowledgements This work was supported by a grant of the National R&D Program for Cancer Control, No. 1210150 Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.ctim.2016.07. 005. References 1. Chang K, Brodie R, Choong M, Sweeney KJ, Kerin MJ. Complementary and alternative medicine use in oncology: a questionnaire survey of patients and health care professionals. BMC Cancer. 2011;11:196. 2. Kim MJ, Lee SD, Kim DR, et al. Use of complementary and alternative medicine among Korean cancer patients. Korean J Intern Med. 2004;19:250–256. 3. Hyodo I, Amano N, Eguchi K, et al. Nationwide survey on complementary and alternative medicine in cancer patients in Japan. J Clin Oncol. 2005;23:2645–2654. 4. John GM, Hershman DL, Falci L, Shi Z, Tsai WY, Greenlee H. Complementary and alternative medicine use among US cancer survivors. J Cancer Surviv. 2016 [Epub ahead of print]. 5. Cao P, Selvan SR, Kupeli Akkol E, Wang N, Yang H, Cheng X. Complementary and alternative medicine in cancer prevention and therapy. Evid Based Complement Altern Med. 2015;2015:639372. 6. Leggett S, Koczwara B, Miller M. The impact of complementary and alternative medicines on cancer symptoms, treatment side effects, quality of life, and survival in women with breast cancer—a systematic review. Nutr Cancer. 2015;67:373–391. 7. Adams KE, Cohen MH, Eisenberg D, Jonsen AR. Ethical considerations of complementary and alternative medical therapies in conventional medical settings. Ann Intern Med. 2002;137:660–664. 8. Tascilar M, de Jong FA, Verweij J, Mathijssen RH. Complementary and alternative medicine during cancer treatment: beyond innocence. Oncologist. 2006;11:732–741. 9. Rockwell S, Liu Y, Higgins SA. Alteration of the effects of cancer therapy agents on breast cancer cells by the herbal medicine black cohosh. Breast Cancer Res Treat. 2005;90:233–239. 10. Sparreboom A, Cox MC, Acharya MR, Figg WD. Herbal remedies in the United States: potential adverse interactions with anticancer agents. J Clin Oncol. 2004;22:2489–2503. 11. Bauml JM, Chokshi S, Schapira MM, et al. Do attitudes and beliefs regarding complementary and alternative medicine impact its use among patients with cancer? A cross-sectional survey. Cancer. 2015;121:2431–2438. 12. Verhoef MJ, Balneaves LG, Boon HS, Vroegindewey A. Reasons for and characteristics associated with complementary and alternative medicine use among adult cancer patients: a systematic review. Integr Cancer Ther. 2005;4:274–286. 13. Kim DY, Kim BS, Lee KH, et al. Discrepant views of Korean medical oncologists and cancer patients on complementary and alternative medicine. Cancer Res Treat. 2008;40:87–92.
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14. Richardson MA, Masse LC, Nanny K, Sanders C. Discrepant views of oncologists and cancer patients on complementary/alternative medicine. Support Care Cancer. 2004;12:797–804. 15. Kim SY, Kim KS, Park JH, et al. Factors associated with discontinuation of complementary and alternative medicine among Korean cancer patients. Asian Pac J Cancer Prev. 2013;14:225–230. 16. Molassiotis A, Fernadez-Ortega P, Pud D, et al. Use of complementary and alternative medicine in cancer patients: a European survey. Ann Oncol. 2005;16:655–663. 17. Shin DW, Roter DL, Cho J, et al. Attitudes toward disclosure of medication side effects: a nationwide survey of Korean patients, caregivers, and oncologists. Psycho-Oncology. 2015;24:1398–1406. 18. National Cancer Institute. Categories of CAM Therapies. National Cancer Institute; [Cited 2015 May, 3]. Available from: http://cam.cancer.gov/health information/categories of cam therapies.htm. 19. Choi JY, Chang YJ, Hong YS, et al. Complementary and alternative medicine use among cancer patients at the end of life: Korean national study. Asian Pac J Cancer Prev. 2012;13:1419–1424. 20. Kim SG, Park EC, Park JH, Hahm MI, Lim JH, Choi KS. Initiation and discontinuation of complementary therapy among cancer patients. J Clin Oncol. 2007;25:5267–5274.
21. Shin JY, Kim SY, Park B, et al. Predictors of complementary and alternative medicine use in cancer care: results of a nationwide multicenter survey in Korea. Evid Based Complement Altern Med. 2012;2012:212386. 22. Shumay DM, Maskarinec G, Gotay CC, Heiby EM, Kakai H. Determinants of the degree of complementary and alternative medicine use among patients with cancer. J Altern Complement Med. 2002;8:661–671. 23. Bishop FL, Lewith G. Who uses CAM? A narrative review of demographic characteristics and health factors associated with CAM use. Evid Based Complement Altern Med. 2010;7:11–28. 24. Helyer LK, Chin S, Chui BK, et al. The use of complementary and alternative medicines among patients with locally advanced breast cancer-a descriptive study. BMC Cancer. 2006;6:39. 25. Bardia A, Barton D, Prokop L, Bauer B, Moynihan T. Efficacy of complementary and alternative medicine therapies in relieving cancer pain: a systematic review. J Clin Oncol. 2006;24:5457–5464. 26. Davis EL, Oh B, Butow PN, Mullan BA, Clarke S. Cancer patient disclosure and patient-doctor communication of complementary and alternative medicine use: a systematic review. Oncologist. 2012;17:1475–1481. 27. Saxe GA, Madlensky L, Kealey S, Wu DP, Freeman KL, Pierce JP. Disclosure to physicians of CAM use by breast cancer patients: findings from the women’s healthy eating and living study. Integr Cancer Ther. 2008;7:122–129.
Contents lists available at ScienceDirect
Complementary Therapies in Medicine journal homepage: www.elsevierhealth.com/journals/ctim
Expected and perceived efficacy of complementary and alternative medicine: A comparison views of patients with cancer and oncologists Sang Hyuck Kim (MD) a , Dong Wook Shin (MD, DrPH, MBA) a,b,∗∗ , You-Seon Nam (MD) c , So Young Kim (MD, PhD) d,e , Hyung-kook Yang (MD) d , Be Long Cho (MD, MPH, PhD) a,b,f,g , Keeho Park (MD, MPH, PhD) h , Heui-Sug Jo (MD, PhD) i , Chang-Yeol Yim (MD, PhD) j , Sin Kam (MD, PhD) k , Jong-Hyock Park (MD, MPH, PhD) d,l,m,∗ a
Department of Family Medicine & Cancer Survivorship Clinic, Seoul National University Hospital, Seoul, Republic of Korea Laboratory of Health Promotion and Health Behavior, Biomedical Research Institute, Seoul National University Hospital, Republic of Korea c Department of Family Medicine, Seoul National University College of Medicine, Seoul, Republic of Korea d National Cancer Control Institute, National Cancer Center, Goyang, Republic of Korea e Regional Cardiocerebrovascular Center, Chungbuk National University Hospital, Cheongju, Republic of Korea f Institute on Aging, Seoul National University College of Medicine, Seoul, Republic of Korea g Advanced Institutes of Convergence Technology, Seoul National University, Suwon, Republic of Korea h Cancer Policy Branch, National Cancer Center, Goyang, Republic of Korea i Department of Health Management and Policy, Kangwon National University School of Medicine, Chuncheon, Republic of Korea j Department of Internal Medicine, Chonbuk National University Medical School, Jeonju, Republic of Korea k Department of Preventative Medicine, School of Medicine, Kyungpook National University, Daegu, Republic of Korea l Department of Health Informatics and Management, College of Medicine, Chungbuk National University, Cheongju, Republic of Korea m Graduate School of Health Science Business Convergence, Chungbuk National University, Cheongju, Republic of Korea b
a r t i c l e
i n f o
Article history: Received 17 March 2016 Received in revised form 15 July 2016 Accepted 29 July 2016 Available online 29 July 2016 Keywords: Complementary and alternative medicine Discrepancy Oncologist Cancer patient Efficacy
a b s t r a c t Background & aims: This study sought to identify discrepancies between the expectations of patients with cancer and oncologists regarding the efficacy of complementary and alternative medicines (CAMs), and to determine how patients evaluate CAM efficacy after its use. Methods: Data from the Cancer Patient Experience Study, a nationwide survey, were used. Seven subdivided efficacy domains were included in the survey. An oncologist-patient matching analysis was done to assess the concordance of CAM efficacies between oncologists and patients with cancer. In addition, the patients’ expectations of CAM efficacies were compared before and after use. Results: Out of 719 participants, 201 patients with cancer (28.0%) reported using CAMs. The patients with cancer generally tended to be more positive about CAM efficacies than the oncologists. The largest discrepancy in efficacy perception was found in the efficacy domain of survival benefit, which included complete disease remission and prolonged survival. Many patients reported that they did not experience the positive efficacy they had anticipated before use. However, a substantial proportion of patients indicated that CAMs were as effective as they had expected, even though there is little evidence supporting the CAM efficacies. Conclusions: There was a marked discrepancy and a lack of concordance in expectations of CAM efficacy between patients with cancer and oncologists. Better communication between the patients and oncologists regarding CAM efficacy would be needed to make the patients to have shared expectations, and to reduce unnecessary CAM use. © 2016 Published by Elsevier Ltd.
1. Introduction ∗ Corresponding author at: College of Medicine/Graduate School of Health Science Business Convergence, Chungbuk National University, Cheongju 28644, Republic of Korea. ∗∗ Corresponding author at: Department of Family Medicine, Seoul National University, College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul 03080, Republic of Korea. E-mail addresses: [email protected] (D.W. Shin), [email protected] (J.-H. Park). http://dx.doi.org/10.1016/j.ctim.2016.07.005 0965-2299/© 2016 Published by Elsevier Ltd.
Currently, the use of complementary and alternative medicines (CAMs) in patients with cancer is widespread and increasing.1–4 Accordingly, an enormous amount of money is being spent in this field.1,2 In a survey conducted in Korea, approximately 78.5% of
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patients with cancer used at least one type of CAM, with a mean monthly cost of $1100 per person.2 However, most clinically implemented CAMs have limited scientific evidence, which is inconclusive to recommend their use.5–7 Even CAMs may induce unwanted negative consequences for conventional cancer treatment, not only directly but also by interfering with the metabolism and the physiological response of conventional treatment.8–10 Therefore, clear communication about CAM use between the patient and their physician is important when deciding on cancer treatment. The use of CAMs is largely driven by expectations of their efficacy by patients with cancer.11,12 Some previous studies revealed that patients with cancer often have much higher expectations of CAM efficacy than physicians.3,13,14 However, these studies did not match the patients with their doctors to assess the concordance of expected CAM efficacies. In addition, experienced efficacy after CAM use are the basis for the decisions of patients with cancer on continued CAM use,15 which can also affect the initiation of CAM usage in other patients with cancer.3,16 Therefore, it is necessary to know how patients evaluate CAM efficacies after their use compared to their initial expectations prior to CAM use. However, to our knowledge, there are no studies comparing the expected efficacies of CAMs with their experienced efficacy after CAM use in patients with cancer. Understanding both the patients’ and physicians’ perspectives on CAMs would help establish better decision making for CAM use. In this study, we compared (1) the expected efficacies of CAMs in patients with cancer and the perceived efficacies of CAMs in their oncologists with a matched patient-physician sample, and (2) the expected and experienced CAM efficacies in patients with cancer before and after use, respectively. 2. Materials and methods 2.1. Study design and subjects This study was conducted as part of the CaPE (Cancer Patient Experience) Study, an annual nationwide survey in Korea, which assesses medical care and treatment options for cancer. This study was supported by the Ministry of Health and Welfare, and conducted by the National Cancer Center. It was approved by the institutional review board of the National Cancer Center (Grant No. 1210150). The survey was conducted in 2012 using oncologist–patient with cancer–caregiver matched triads, to explore the different views of oncologists, cancer patients and family caregivers in medical care and treatment. Trained nurses helped the participants to complete and understand the survey questionnaires. The detailed process for recruiting oncologists, patients with cancer, and their caregiver has been described previously.17 Briefly, a total of 144 board-certified oncologists were recruited from 13 cancer centers. Each oncologist was asked to recruit 6 consecutive patients who were accompanied at the visit by a family caregiver. Among the 144 oncologists, 134 completed the study survey (93.1% participation rate). From the 960 patients, 725 dyads and their caregivers completed the survey (75.5% participation rate). 2.2. Survey questionnaires The CAM questionnaire was administered only to patients and physicians, in order to have matched analyses. The English version of the survey questionnaires is provided as online-only Supplementary material. The patients were first asked whether they had ever used CAMs after their cancer diagnosis for cancer care. If the answer
was ‘Yes. But not now’ or ‘Yes. I am currently using’, they were asked to describe the type of CAM used. We presented 8 CAM categories in the survey questionnaire, which are designated as CAM Therapies by the Office of Cancer Complementary and Alternative Medicine, The National Cancer Institute (NCI)18 : (1) Alternative Medical System (e.g., acupuncture, moxa cautery, cupping therapy, ayurveda, traditional Chinese medicine, homeopathy, naturopathy); (2) Energy/Exercise Therapy (e.g., tai chi, qi gong, yoga); (3) Manipulative and Body-Based Methods (e.g., chiropractic manipulation, massage, osteopathic manipulation); (4) Mind-Body Interventions (e.g., meditation, hypnosis, biofeedback, imagery, relaxation, music therapy, aromatherapy); (5) Spiritual Therapies (e.g., intercessory prayer and spiritual healing); (6) Dietary Therapy (e.g., vegetarian diet, Gerson diet); (7) Nutritional Therapeutics (e.g., vitamin, melatonin, mineral supplement, herb and herbal extract); and (8) Others. Some category modifications were made to take into account the prevalence and general concept of CAMs in Korea. For example, energy and exercise therapy were combined into a single category since Koreans tend not to conceptually distinguish these two examples. Dietary therapy and nutritional therapeutics were separated, as many Koreans do not equate specific dietary therapy and nutritional supplements. The ‘pharmacological and biologic treatments’ NCI category was not included in the response options, since these treatments (e.g., antineoplastions, 714X, low dose naltrexone) are generally not available or practiced in Korea. Since patients could use more than one CAM type, multiple responses were allowed. The patients were asked about their expectations on CAM efficacies before use on the following items: (1) complete remission of disease; (2) life prolongation; (3) pain or symptom relief; (4) regaining physical strength; (5) immune function improvement; (6) psychological and emotional support for the patient; and (7) psychological and emotional support for their family caregivers. Response options were yes or no. Simultaneously, they were also asked whether they experienced CAM efficacy on the same items after CAM use. Finally, the patients were asked if they had discussed about CAM use with doctors. The physicians were asked about their opinions on the general efficacy of CAMs using the same set of questions. Also, they were asked if they had discussed about CAM use with their patients. In addition, the survey collected the respondents’ sociodemographic and medical information. Further, the primary cancer diagnosis using the Surveillance, Epidemiology, and End Results (SEER) stage criteria was retrieved from the hospital information systems of each participating center.
2.3. Statistical analysis A descriptive analysis was performed for the respondents’ baseline characteristics. We compared the proportions of positive responses to the expected efficacy items in both medical oncologists and surgical oncologists. Radiotherapy oncologists were excluded in the analysis due to possible bias by the small sample size of included radiotherapy oncologists (n = 7). The proportion of positive responses to the expected efficacy items from the oncologists and the patients was compared using a chi square test. After matching the patients to their own doctor (multiple patients with cancer could be matched to a single oncologist), a Cohen’s Kappa and the p values from the McNemar test were calculated to assess the concordance of the responses between the oncologist and their own patients. The proportions of positive response to items regarding the expected and experienced CAM efficacies were compared using a McNemar test. All statistical analyses were conducted using STATA software version 14.0 (StataCorp., TX). A p value of less than 0.05 was considered statistically significant.
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Table 1 Respondents’ Characteristics According to the Experience of CAM use (n, %). Ever Useda (n = 201) Mean Age (SD) Sex Male Female
P value†
Never Used (n = 518)
59.4
(12.8)
60.5
(12.8)
0.267
87 114
(43.3) (56.7)
242 276
(46.7) (53.3)
0.407
Educational Status <9 years 9–12 years >12 years Missing
78 66 56 1
(38.8) (32.8) (27.9) (0.5)
265 167 82 4
(51.2) (32.2) (15.8) (0.8)
0.001
Monthly Income (KRW) <2 million ≥2 million Missing
110 88 3
(54.7) (43.8) (1.5)
310 203 5
(59.9) (39.2) (1.0)
0.236
Cancer Type (Primary) Stomach Lung Liver Colon Breast Cervix Others
21 27 14 44 39 12 44
(10.5) (13.4) (7.0) (21.9) (19.4) (6.0) (21.9)
97 70 38 85 63 37 128
(18.7) (13.5) (7.3) (16.4) (12.2) (7.1) (24.7)
0.023
Treatment Situation Under Initial Treatment On Regular Follow-up after Treatment On Regular Follow-up after Cure Under Treatment for Metastasis of recurrence Do Not Know Others (Ex. Treatment for Second Primary Cancer) Missing
76 74 18 29 3 1 0
(37.8) (36.8) (9.0) (14.4) (1.5) (0.5) (0.0)
246 161 21 76 11 2 1
(47.5) (31.1) (4.1) (14.7) (2.1) (0.4) (0.2)
0.047‡
SEER Stage at the Time of Diagnosis In Situ or Local Regional Distant Unknown/Missing
80 75 42 4
(39.8) (37.3) (20.9) (2.0)
210 199 99 10
(40.5) (38.4) (19.1) (1.9)
0.948‡
CAM, complementary and alternative medicine; KRW, Korean Won; SEER, Surveillance, Epidemiology, and End Results Program. a Respondents who were using or previously used CAMs after cancer diagnosis for cancer care were included. † t-test for continuous variables and chi-square test for categorical variables. ‡ Obtained from the Fisher’s exact test.
3. Results 3.1. Patient experiences with CAM use and oncologist characteristics Table 1 provides the baseline patient characteristics. Among the original 725 patients with cancer who participated in the CaPE Study, 719 (99.2%) answered the questionnaire regarding their CAM usage. Among these, 140 patients (19.5%) responded that they were using at least one type of CAM at the time of the survey, and 61 patients (8.5%) reported that they had previously used at least one type of CAM after cancer diagnosis for cancer care but were not currently using it. The majority of the respondents had never used CAMs. Higher educational status, cancer type (e.g. stomach, colon, and less common cancers), and treatment situation were significantly associated with CAM. However, other characteristics including age, sex, monthly income, and SEER stage at the time of diagnosis were not significantly associated with CAM use. Table 2 indicates the patient usage in each CAM category. Among the 201 patients who had used a CAM after their cancer diagnosis, the majority of patients reported they had used nutritional or dietbased therapies. A relatively small proportion of patients had used mind-body interventions, spiritual therapy, or manipulative and body-based methods A total of 134 oncologists participated in the CaPE Study. Their subspecialties included medical oncology (n = 59, 44.0%), surgical oncology (n = 68, 50.7%), and radiotherapy (n = 7, 5.2%). The
Table 2 Categories of CAMs Used By Patients (n, %). Alternative Medical System Energy/Exercise Therapy Manipulative and Body-Based Methods Mind-Body Interventions Spiritual Therapies Dietary Therapy Nutritional Therapeutics Others
45 74 13 26 23 112 126 1a
(22.4) (36.8) (6.5) (12.9) (11.4) (55.7) (62.7) (0.5)
CAM, complementary and alternative medicine. Total number of respondents who used CAMs was 201. a Using electric potential therapy device.
efficacy of CAMs on immune function improvement was significantly different across the oncologists’ subspecialties, with no significant differences in the other expected efficacies (Table 3). 3.2. Patients’ expected efficacy and physician’s perceived efficacy of CAMs: a comparison of the patients’ and oncologists’ views The comparison of efficacies expected by patients with cancer and the oncologists’ perceived efficacies of CAMs are shown in Fig. 1. More than half of the patients expected positive efficacy with CAM use regarding complete remission of their disease, life prolongation, pain or symptom relief, and psychological and emotional support for their family caregivers. Moreover, approximately 80% of patients with cancer expected CAMs to be efficacious in
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Table 3 Oncologists’ Expected Efficacies of CAMs Grouped according to Their Specialties (n, %). Medical Oncologist (n = 59).
Surgical Oncologist (n = 68)
Radiotherapy Oncologist (n = 7)
Yes
Yes
Yes
No
No
P valuea
No
Complete Remission of Disease (n = 134) Life Prolongation (n = 134) Pain or Symptom Relief (n = 134) Regaining physical strength (n = 134) Immune Function Improvement (n = 134)
2 3 35 24 21
(3.4) (5.1) (59.3) (40.7) (35.6)
57 56 24 35 38
(96.6) (94.9) (40.7) (59.3) (64.4)
3 6 50 39 37
(4.4) (8.8) (73.5) (57.4) (54.4)
65 62 18 29 31
(95.6) (91.2) (26.5) (42.6) (45.6)
0 0 4 5 5
(0.0) (0.0) (57.1) (71.4) (71.4)
7 7 3 2 2
(100.0) (100.0) (42.9) (28.6) (28.6)
1.000 0.698 0.208 0.090 0.043
Psychological and Emotional Support For Patient (n = 134) For Family Caregivers (n = 134)
54 48
(91.5) (81.4)
5 11
(8.5) (18.6)
63 58
(92.6) (85.3)
5 10
(7.4) (14.7)
7 7
(100.0) (100.0)
0 0
(0.0) (0.0)
1.000 0.622
CAM; complementary and alternative medicine. a Obtained from the chi-square test or Fisher’s exact test as appropriately.
Fig. 1. Patients’ and Doctors’ Expected CAM Efficacies. All of the 134 doctors responded to the each efficacy category. The total numbers of the cancer patients in each category were different due to different response rates (complete remission of disease, n = 195; life prolongation, n = 194; pain or symptom relief, n = 193; regaining physical strength, n = 195; immune function improvement, n = 196; psychological and emotional support for patient, n = 194; psychological and emotional support for family caregivers, n = 193). All p values from the t-test were below 0.001, except for RPS (p = 0.070) and PESFC (p = 0.001).
regaining physical strength, immune function improvement, and psychological and emotional support for the patient. Unlike the patients’ responses, very few oncologists viewed CAMs as an efficacious treatment for the complete remission of disease (n = 5, 3.7%) and life prolongation (n = 9, 6.7%). Approximately half of the oncologists endorsed CAMs for their positive efficacy in pain or symptom relief, regaining physical strength, and immune function improvement. For these items, patients’ expectation were significantly higher than the perceived efficacy by oncologists, except for pain or symptom relief (p = 0.070). In contrast, the oncologists were highly positive regarding efficacies of CAMs for the psychological and emotional support of the patient, and for the family caregivers. These measures were significantly higher than the measures of patients’ expectations.
We performed a doctor-patient matching analysis to assess the concordance of expected CAM efficacies between the oncologists and patients (Table 4). A total of 134 oncologists were matched to their own patients. Agreement rates for Complete Remission of Disease, life prolongation, relief of pain or symptoms, reinforcement of physical strength, immune function improvement, psychological and emotional support for patients and families were 44.6%, 46.9%, 53.4%, 55.4%, 57.1%, 73.2%, and 66.3%, respectively. No significant concordance was observed between the patients’ expected efficacy and the oncologists’ perceived efficacy. The highest kappa was 0.156 for immune function improvement. P values from the McNemar test were below 0.001 in all efficacies of CAMs except for the relief of pain or symptom (p = 0.011).
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Table 4 Doctor-Patient Matching Analysis about CAMs’ Efficacy (n, %). Doctors’ Expected Efficacy Patients’ Expected Efficacy
Yes
No
Agreement (%)
kappa (SE)a
†
P value
Complete Remission of Disease
Yes No
6 3
(3.1) (1.5)
105 81
(53.8) (41.5)
87
(44.6)
0.016 (0.026)
<0.001
Life Prolongation
Yes No
7 5
(3.6) (2.6)
98 84
(50.5) (43.3)
91
(46.9)
0.010 (0.032)
<0.001
Relief of Pain or Symptoms
Yes No
76 57
(39.4) (29.5)
33 27
(17.1) (14.0)
103
(53.4)
0.019 (0.070)
<0.011
Reinforcement of Physical Strength
Yes No
85 14
(43.6) (7.2)
73 23
(37.4) (11.8)
108
(55.4)
0.099 (0.057)
<0.001
Immune Function Improvement
Yes No
80 15
(40.8) (7.7)
69 32
(35.2) (16.3)
112
(57.1)
0.156 (0.060)
<0.001
Psychological and Emotional Support Yes For Patient No
139 40
(71.6) (20.6)
12 3
(6.2) (1.5)
142
(73.2)
0.013 (0.060)
<0.001
Yes No
112 46
(58.0) (23.8)
19 16
(9.8) (8.3)
128
(66.3)
0.128 (0.067)
<0.001
For Family Caregivers
CAM, complementary and alternative medicine; SE, standard error. The total numbers of the cancer patients in each category were different due to different response rates. 134 oncologists matched to their own patients. a Cohen’s kappa after doctor-patient matching. † Obtained from the McNemar test.
3.3. Expected efficacy and self-reported efficacy after use: patients’ view Fig. 2 shows the comparison of the expected efficacy and the self-reported efficacy after use in patients with cancer. Generally, the proportions of positive CAM efficacies after use were lower than those of the expected efficacies before use. However, a substantial proportion of patients thought that CAMs were effective for the complete remission of diseases (before use: 58.3%; after use: 35.3%; p = 0.001), life prolongation (before use: 55.4%; after use: 33.9%; p = 0.001), and pain or symptom relief (before use: 58.4%; after use: 42.2%; p = 0.001). More than half of the patients reported a positive effect for CAMs on regaining physical strength, immune function improvement, and psychological and emotional support for patients, and for family caregivers.
3.4. Experience of counseling for CAM use One third of cancer patients (n = 71, 35.9%) in the present study had indicated that they did not counsel about CAM use with their doctors. Only 23.9% (n = 32) of oncologists in the present study reported that they had discussed about CAM use with their patients.
4. Discussion To our knowledge, this is the first study which compared expected efficacies of CAMs among cancer patients with those among the oncologists, as well as with self-reported experienced efficacies after use. Our study design employed doctor-patient matching and pre- and post-CAM use matching, which enabled us to explore the difference in viewpoints between the patients and their physicians in a clinical setting as well as the dynamic shift of the patients’ perspective on their perceived efficacy of CAMs. Additional strengths of this study include systematic sampling methods with a high response rate, supporting the generalizability of these results across the Korean population.
4.1. Use of CAMs in Korean cancer patients In this study, approximately 28.0% of patients with cancer reported CAM use. This figure is much lower than those in previous reports on CAM prevalence in Korea.2,13,19,20 This may be due to the differences in CAM definitions. For example, one previous study presented ‘mushroom’ and ‘honey’ as examples of CAMs, while ours did not include such a definition.20 In addition, there may be differences in the response rate, the included cancer centers, and the characteristics of the patients with cancer included in this study. However, the reported prevalence of CAM use in this study is similar to that found in our 2008 survey, which was conducted in 10 cancer centers (the prevalence of CAM use was 25.5%).21 Like many other studies, the most frequently used CAM type was diet-based and included food supplements, such as herbs and herbal extracts.2,15,19 A considerable proportion of respondents used energy/exercise therapy. In this study, a higher educational status, colon or breast cancer diagnosis, and treatment situation (e.g., ‘on regular follow-up after treatment’) were significantly associated with CAM use. A higher educational status has been consistently identified as a factor associated with higher CAM use in patients with cancer.16,22,23 While the reasons for this association are not clear, some studies suggest that the relatively sufficient financial resources enable this population to bear the additional cost of CAMs.20,23 The reason for higher CAM use in patients with colorectal or breast cancer could not be determined by our study design. However, a previous study suggested different patterns of CAM use among patients with different cancer types.20 Additionally, patients who were on regular follow-up after treatment showed higher prevalence of ever CAM use than who were on initial treatment. One possible reason could be that patients who had finished initial treatment felt the urge to do “something” for their health, and seek CAM use. However, further studies are needed to address this question. 4.2. The discrepant view between patients with cancer and oncologists regarding CAM efficacy Consistent with previous studies,3,13,14 this study showed a marked discrepancy between the expectations of patients with
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Fig. 2. Expected and Self-Reported CAM Efficacies in Patients with Cancer. The total numbers of the respondents in each category were different due to different response rates (complete remission of disease, n = 187; life prolongation, n = 186; pain or symptom relief, n = 185; regaining physical strength, n = 190; immune function improvement, n = 190; psychological and emotional support for patient, n = 189; psychological and emotional support for family caregivers, n = 186). All p values from the McNemar test were below 0.001, except for psychological and emotional support for patient (p = 0.028), and psychological and emotional support for family caregivers (p = 0.289).
Table 5 Patients’ Expected Effects of CAMs grouped according to the SEER Stage at the Time of Diagnosis (n, %). In Situ or Local
Regional
Yes
Yes
No
Distant No
Yes
Unknown/Missing No
Yes
P valuea
p for trend
No
Complete Remission of Disease (n = 195) Life Prolongation (n = 194) Pain or Symptom Relief (n = 193) Regaining physical strength (n = 195) Immune Function Improvement (n = 196)
37 32 35 62 56
(48.1) (41.6) (46.1) (80.5) (72.7)
40 45 41 15 21
(51.9) (58.4) (53.9) (19.5) (27.3)
46 45 46 61 59
(63.0) (61.6) (63.9) (84.7) (80.8)
27 28 26 11 14
(37.0) (38.4) (36.1) (15.3) (19.2)
25 25 24 32 30
(61.0) (62.5) (58.5) (76.2) (71.4)
16 15 17 10 12
(39.0) (37.5) (41.5) (23.8) (28.6)
3 3 4 3 4
(75.0) (75.0) (100.0) (75.0) (100.0)
1 1 0 1 0
(25.0) (25.0) (0.0) (25.0) (0.0)
0.147 0.022 0.084 0.523 0.403
0.111 0.014 0.107 0.702 0.925
Psychological and Emotional Support For Patient (n = 194) For Family Caregivers (n = 193)
60 48
(78.9) (63.2)
16 28
(21.1) (36.8)
56 50
(76.7) (69.4)
17 22
(23.3) (30.6)
32 30
(78.0) (73.2)
9 11
(22.0) (26.8)
3 3
(75.0) (75.0)
1 1
(25.0) (25.0)
0.947 0.502
0.867 0.248
SEER, Surveillance, Epidemiology, and End Results Program. The total numbers of the respondents in each category were different due to different response rates. The respondents whose SEER stages were ‘Unknown/Missing’ were excluded for the calculation of the p-values and the p for trend. a Obtained from the chi-square test.
cancer regarding CAM efficacy and the perception of the oncologists. Since patients were generally positive regarding CAM efficacy, it is possible that many patients used a CAM treatment that their own physician did not think was effective. The largest discrepancy was observed within the domain of complete remission of disease or prolonged survival. In particular, patients with more advanced cancer stages were more likely to expect life prolongation (Table 5 p for trend = 0.014). A previous study suggested that patients with cancer believed that CAMs could replace conventional treatment in advanced cancer stages.24 On the other hand, most oncologists were aware that there is currently minimal evidence for improved survival from any CAM therapy.5,7,25 In this study, the oncologists supported the use of CAM as helpful for the patients’ psychological and emotional support. These discrepancies should be addressed
during treatment consultations, regardless of the patients’ actual CAM usage. The lack of concordance revealed by our unique matched analysis suggests that patients and their physicians do not share common views before treatment initiation. Previous studies have suggested that a substantial proportion of patients with cancer do not disclose CAM use to their doctors,26,27 and that oncologists are generally not willing to have conversations about CAMs with their patients.13,26 Similarly, in our study many patients who ever used CAM said that they did not counsel about CAM use with their doctors. Furthermore, only a minority of oncologists in the present study reported that they had discussed about CAM use with their patients. Such a lack of conversation about CAMs may lead to discrepant views between the patients and their physicians, inadequate decision
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making about CAM use, and even harmful effects for the patients. This highlights the need for better communication between the oncologists and their patients regarding the CAM use to provide better guidance for patients. Even if the existing evidences are not enough, oncologists need to discuss with their patients about possible benefits and harms of CAM.
Finally, the present study is a cross-sectional survey, and is susceptible to recall bias. The response about their past thinking could be affected by what occurred after that. A prospective study might be needed to overcome such bias.
4.3. Patients’ perception of actual benefit after CAM use
In conclusion, our study showed a marked discrepancy and a lack of concordance between the expectations of patients with cancer regarding CAM’s efficacy and the perception of the oncologists. In addition, we found that a substantial proportion of patients believed that CAMs were as effective as they had expected. Considering low consultation rate of CAM use, better communication between the patients and oncologists regarding CAM efficacy would be needed to make the patients to have shared expectations, and to reduce unnecessary CAM use.
Many patients with cancer reported that they did not actually experience the positive CAM efficacies they expected before use. This was most evident when the patients expected a physical effect after CAM use, such as complete remission, life prolongation, or pain and symptom relief. However, a substantial proportion of patients indicated that CAMs were as effective as they had expected. Despite the limited scientific evidence of CAMs,5,7–10 there may be some unmet needs contributing to the expected and experienced CAM efficacies in patients with cancer.13 To identify and to fill such needs can improve patients’ quality of life and their satisfaction of cancer treatment. Further studies to investigate on this are needed. Validating the patients’ perception about the experienced efficacy is beyond the scope of our study. Nevertheless, a subjective, positive experience may lead to the continuation of CAM use,15 and even a recommendation of CAM use to other patients.3,16 Therefore, our findings suggest that patients’ beliefs about CAMs are not easily modified by a simple description of CAMs as ineffective. While oncologists need to provide evidence-based information about CAMs, they should not discourage or disapprove CAM use, but rather listen to the patient’s needs, worries, and intents behind CAM use. Otherwise, the discrepancy in the oncologists’ views on CAM efficacy can lead to patients’ concealment of CAM use to their physician. Integrative oncology programs, which have been established in several cancer centers, may provide evidence-based information and support for making appropriate decision regarding CAM use.11 One notable limitation of this study is the discrete categorization of various CAMs. In fact, CAMs in the same category may have different efficacies. Furthermore, many patients with cancer may use various types of CAMs. Therefore, if specific types, rather than categorization of CAMs were used, we may have obtained different results. However, since we used CAM categorization, the general perception about the various CAMs could be evaluated. Second, we presented only “Yes” or “No” as answer choices. More options, such as a Likert-type scale, may enable a more sensitive evaluation of the different expectations between cancer patients and oncologists. Nonetheless, the different expectations about CAM efficacy in the present study are consistent with previous studies.3,13,14 Therefore, the possible limitations of the presented choices might be minimal. Third, as the present study focused on the efficacies of CAM, questionnaires regarding possible harms of CAM were not included in the survey. As expected or experienced harms of CAM can affect initiation or continuation of CAM use, further studies are needed to address this issue. Fourth, we did not take into account the duration of CAM use. The efficacy domains of “Complete remission of disease” and “Life prolongation” need several years for patients with cancer to be able to say conclusively that they are in remission or have had survival benefits. In addition, if patients were using CAMs simultaneously with conventional cancer treatment, it could be very difficult for cancer patients to distinguish the different efficacies of CAMs and conventional cancer treatments. However, the study design of the present study, which dealt with CAM efficacy before and after CAM use, may be enough to identify cancer patients’ positive view regarding CAM efficacy even in the remission of the disease and life prolongation.
5. Conclusion
Conflict of interest statement The authors have no potential conflicts of interest. Acknowledgements This work was supported by a grant of the National R&D Program for Cancer Control, No. 1210150 Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.ctim.2016.07. 005. References 1. Chang K, Brodie R, Choong M, Sweeney KJ, Kerin MJ. Complementary and alternative medicine use in oncology: a questionnaire survey of patients and health care professionals. BMC Cancer. 2011;11:196. 2. Kim MJ, Lee SD, Kim DR, et al. Use of complementary and alternative medicine among Korean cancer patients. Korean J Intern Med. 2004;19:250–256. 3. Hyodo I, Amano N, Eguchi K, et al. Nationwide survey on complementary and alternative medicine in cancer patients in Japan. J Clin Oncol. 2005;23:2645–2654. 4. John GM, Hershman DL, Falci L, Shi Z, Tsai WY, Greenlee H. Complementary and alternative medicine use among US cancer survivors. J Cancer Surviv. 2016 [Epub ahead of print]. 5. Cao P, Selvan SR, Kupeli Akkol E, Wang N, Yang H, Cheng X. Complementary and alternative medicine in cancer prevention and therapy. Evid Based Complement Altern Med. 2015;2015:639372. 6. Leggett S, Koczwara B, Miller M. The impact of complementary and alternative medicines on cancer symptoms, treatment side effects, quality of life, and survival in women with breast cancer—a systematic review. Nutr Cancer. 2015;67:373–391. 7. Adams KE, Cohen MH, Eisenberg D, Jonsen AR. Ethical considerations of complementary and alternative medical therapies in conventional medical settings. Ann Intern Med. 2002;137:660–664. 8. Tascilar M, de Jong FA, Verweij J, Mathijssen RH. Complementary and alternative medicine during cancer treatment: beyond innocence. Oncologist. 2006;11:732–741. 9. Rockwell S, Liu Y, Higgins SA. Alteration of the effects of cancer therapy agents on breast cancer cells by the herbal medicine black cohosh. Breast Cancer Res Treat. 2005;90:233–239. 10. Sparreboom A, Cox MC, Acharya MR, Figg WD. Herbal remedies in the United States: potential adverse interactions with anticancer agents. J Clin Oncol. 2004;22:2489–2503. 11. Bauml JM, Chokshi S, Schapira MM, et al. Do attitudes and beliefs regarding complementary and alternative medicine impact its use among patients with cancer? A cross-sectional survey. Cancer. 2015;121:2431–2438. 12. Verhoef MJ, Balneaves LG, Boon HS, Vroegindewey A. Reasons for and characteristics associated with complementary and alternative medicine use among adult cancer patients: a systematic review. Integr Cancer Ther. 2005;4:274–286. 13. Kim DY, Kim BS, Lee KH, et al. Discrepant views of Korean medical oncologists and cancer patients on complementary and alternative medicine. Cancer Res Treat. 2008;40:87–92.
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