J Complement Integr Med. 2014; 11(4): 297–303
Zane R. Gallinger and Geoffrey C. Nguyen*
Practices and attitudes toward complementary and alternative medicine in inflammatory bowel disease: a survey of gastroenterologists Abstract Background: Use of complementary and alternative medicine (CAM) is increasingly prevalent among patients with inflammatory bowel disease (IBD). We sought to characterize the practices and attitudes of IBD physician providers toward CAM. Methods: A web-based survey was sent to non-trainee physician members of the American Gastroenterological Association with an interest in IBD. The survey included multiple-choice and Likert scale questions which queried physician perceptions of CAM and their willingness to discuss CAM with patients. Results: The vast majority of respondents (80%) considered themselves IBD subspecialists with 75% holding academic appointments. Nearly a third reported initiating conversations on CAM in the majority of their patient interactions, while 90% perceived that a majority of their patients were reluctant to bring up the topic of CAM. Nearly three quarters (72%) of respondents felt comfortable discussing CAM, while those that did not most frequently cited lack of knowledge as the reason. More than half (55%) stated they had no systematic approach to discussing CAM. Most gastroenterologists (65%) reported no formal training in CAM. Most gastroenterologists had recommended use of probiotics, and nearly half had recommended acupuncture. A vast majority believed that there was adjunctive role for CAM in treatment of IBD. Conclusions: Academic IBD specialists were receptive to the use of CAM, and most felt that it had a role in the treatment of IBD, without necessarily compromising conventional therapy. Formal educational initiatives and societal recommendations on the use of CAM may facilitate a more systematic approach to its use in daily practice. *Corresponding author: Geoffrey C. Nguyen, Mount Sinai Hospital Centre for Inflammatory Bowel Disease, University of Toronto, Toronto, ON, Canada; University of Toronto, Department of Medicine, Toronto ON, Canada, E-mail: [email protected] Zane R. Gallinger, University of Toronto, Department of Medicine, Toronto ON, Canada
Keywords: complementary and alternative medicine, Crohn’s disease, inflammatory bowel disease, ulcerative colitis DOI 10.1515/jcim-2014-0008 Received February 16, 2014; accepted August 29, 2014; previously published online October 7, 2014
Introduction The use of complementary and alternative medicine (CAM) has risen steadily across many countries over the past few decades [1–5]. While once considered an unconventional modality, CAM is now a multibillion-dollar industry. The National Center for Complementary and Alternative Medicine, a part of the National Institute of Health (NIH), reported that Americans spent nearly $34 billion on CAM in 2008 alone. Originally a therapy considered popular only among fringe demographics, the characteristics of individuals who use CAM appear to be narrowing [6]. Nonetheless, patients with specific diseases continue to use CAM more than others [7, 8]. One group known to use CAM at higher rates than the general population are those with inflammatory bowel disease (IBD), with some studies showing that nearly half of all IBD populations have used CAM [5, 6, 9]. The generally chronic course of IBD, the lack of consistently effective traditional therapies, as well as patients desire to gain control over their illness, are reasons that some have suggested IBD patients use CAM at high rates [10, 11]. Multiple educational resources exist for patients to access information on CAM, however it remains unclear if patients consider their physicians a reliable resource for information on CAM [12]. As CAM use rises, it can be expected that physicians will be increasingly relied upon to provide information to patients that seek advice on this treatment modality. Physicians have, however, been reluctant to engage in this topic because of lack of clinical trial data and government regulation [13]. Moreover, adverse interactions between CAM and conventional therapies prescribed by physicians have been described [14]. The above concerns
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Gallinger and Nguyen: A survey of gastroenterologists
may lead to uncertainty about CAM, and subsequently poor communication with patients. Nonetheless, the number of medical schools in the United States that have incorporated CAM-related medical education in their curriculum rose from 46 in 1996–1997 to 82 in 1999–2000 [15]. Given its increasing popularity, in addition to a new focus from medical schools, CAM will likely remain a relevant component of the physician–patient relationship. An understanding of physician’s perceptions of CAM and how they interact with their patients during conversations on this topic are critical in developing CAM-related educational initiatives. The purpose of this study was to examine factors that influence the relationship between gastroenterologists and patients when CAM is discussed and to assess areas of CAM that gastroenterologists feel require further focus. The results will help inform which elements of CAM require increased attention by academic and professional institutions.
Methods
questionnaire consisted of 3 screening questions for eligibility and an additional 15 questions with binary and scaled answers. A combination of contingency, matrix, and close-ended questions is used. Participants were also asked to select on a 7-point Likert scale their level of agreement or disagreement among a series of statements querying their perceptions of and practices related to CAM.
Survey administration and data collection An invitation to participate in the survey was sent to all members of the AGA who were affiliated with the Immunology, Microbiology, and IBD section. The questionnaire was administered using an online survey engine (Novi-Survey). Five separate e-mails were sent to non-responders after the initial invitation in 1-month intervals. Participants who selected the link to the survey site were given an explanation of the study, and consent was implied if participants proceeded to the survey. All respondents were anonymously assigned a unique identifier, and table and graphs were created using Microsoft Excel.
Study population Ethics approval All gastroenterologists who were members of the American Gastroenterological Association (AGA), and were affiliated with the IBD sub-section, were invited to participate. Additional inclusion criteria included being a practicing physician having cared for IBD patients in the prior 12 months and having had completed medical, specialty, and/or subspecialty training.
The study protocol was approved by the Research Ethics Board at Mount Sinai Hospital, Toronto, Ontario.
Results Study population
Study design and content We distributed a questionnaire to gastroenterologists to assess their opinions and practices toward patients who use CAM. The questionnaire was reviewed and critiqued by IBD specialists to increase its face validity. Although there is no universally accepted definition of CAM, the National Center for Complementary and Alternative Medicine broadly defines it as “diverse medical and healthcare systems, practices, and products not considered as conventional medicine” [16]. In our survey, CAM referred to agents, which included, but were not limited to meditation, acupuncture, traditional Chinese medicine, probiotics, massage, and herbal diets. The
There were 95 respondents to the survey which translated into an approximately 10% response rate. A total of 78 of respondents met inclusion criteria. Three quarters of respondents practiced in an academic setting or had an academic appointment. The mean length of time in practice was 17 years (standard deviation (SD), 12.5 years; Table 1). The majority of respondents (80%) considered themselves IBD subspecialists. However, 60% reported having less than 50% of their practice comprised IBD patients. The vast majority of respondents (80%) suggested that adult gastroenterology (GI) was their primary practice, while 17% practiced pediatric GI (Table 1).
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Gallinger and Nguyen: A survey of gastroenterologists
Table 1
Practice characteristics of respondents n (%).
Years in practice, mean SD
17.4 12.5
Primary practice setting Academic Community Both Scope of practice Limited to adult gastroenterology Gastroenterology and internal medicine Pediatric gastroenterology Surgery Other Percentage of gastroenterology practice patients with IBD < 10 10–25 25–50 > 50 Considered self-subspecialist in IBD Yes No
49 (63) 20 (26) 9 (12) 62 (79) 2 (2) 13 (17) 0 (0) 1 (1)
16 (20) 24 (31) 10 (13) 28 (36) 62 (80) 16 (20)
Patient–physician interactions related to CAM When queried about interactions with their patients on the topic of CAM, approximately one third (29%) of respondents reported that they independently initiated a discussion on CAM with over half of their patient population. A vast majority of gastroenterologists (90%) reported that less than half of their patient population initiated a discussion on CAM. Similarly, a minority of (14%) gastroenterologists believed that more than one half of their patients had mentioned their use of CAM as part of treatment for their IBD. Only 12% of gastroenterologists believed that a majority of their patients use CAM without keeping their physicians informed (Table 2). Sixty-eight percent of
Table 2
physicians believed their potential disapproval was the reason patients withheld information on their use of CAM.
Comfort level and CAM Nearly three quarters of respondents (72%) felt comfortable or very comfortable discussing CAM with their patients (Figure 1A). The most common reasons for discomfort with discussing CAM were lack of knowledge and the belief that it was not useful (Figure 1B). The majority of gastroenterologists (65%) had never received any formal training about CAM. Just over a third of gastroenterologists reported training in CAM with the majority gaining exposure through continued medical education sessions (55%) while other received training through independent learning (22%), medical school (15%), and hospital workshops (7%). Over half of gastroenterologists (55%) acknowledged that their response to patient CAM use varied from individual to individual. An additional 30% reported that they are willing to participate in the initial discussion about CAM with their patients, while 10% actively recommend CAM once their patients have engaged them in conversation. No gastroenterologists dismissed CAM outright, and one was willing to refer their patients to an alternative practitioner.
Types of CAM The majority of gastroenterologists had heard of the various forms of CAM listed (Figure 2), with the exception of wormwood, Boswellia serrata, and Andrographis paniculata. Figure 2 shows the forms of CAM recommended by gastroenterologists with probiotics (86%) and acupuncture (47%) being the most commonly cited (Figure 2).
Responses to specific questions surrounding interactions with patients and CAM use n (%).
What percentage of your patients has mentioned the use of CAM as a part of their treatment of IBD? How often do you initiate a discussion with your patients about their use of CAM? How often does a patient with IBD initiate a discussion about their use of CAM? What percentage of your patients do you think use CAM and do not tell you about it?
299
< 10%
10–25%
25–50%
21 (27)
27 (35)
19 (24)
11 (14)
19 (24)
19 (24)
17 (19)
23 (29)
19 (25)
30 (39)
20 (26)
8 (10)
23 (29)
24 (31)
22 (28)
9 (12)
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> 50%
300
Gallinger and Nguyen: A survey of gastroenterologists
Figure 1 Comfort levels and CAM. (A) Comfort levels of gastroenterologists when discussing CAM with their patients. (B) Reason that respondents were not comfortable or only somewhat comfortable discussing CAM with patients.
Figure 2 Gastroenterologists’ familiarity with and recommendation practices for specific modalities of CAM. Black bars the proportion of respondents who were familiar with a specific type of CAM and gray bars represent the proportion who recommended that specific modality.
Gastroenterologist beliefs about CAM Table 3 displays responses by gastroenterologists about their beliefs and attitudes toward CAM. The majority believed that their patients would pursue CAM despite their recommendations for or against it. Respondents felt there needed to be more regulatory oversight of CAM and more studies to demonstrate its efficacy. Most gastroenterologists believed that patients who responded poorly to conventional IBD medical therapy most often used CAM. Half of the physicians surveyed did not believe that CAM would interfere with adherence to medical management of IBD, while 20% were not sure. A vast
majority of respondents believed that CAM could play an important adjunctive role in the treatment of IBD.
Discussion This survey study described the approach and beliefs of American gastroenterologists toward CAM and how these attitudes influenced their interactions with patients that use CAM to treat IBD. As the popularity and use of CAM increase, physicians will continue to be tasked with the responsibility of discussing merits and drawbacks of CAM with their patients. We believe it is important to gain an
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Gallinger and Nguyen: A survey of gastroenterologists
Table 3
301
Perceptions of CAM efficacy, user characteristics, and utility in patients that use it to treat IBD n (%).
Patients who have poor response to conventional IBD therapy tend to use more CAM My patients will pursue CAM despite my recommendations for or against it Women, high income, and high education patients are more likely to use CAM My patients would benefit from a wellness center at my institution that could provide access to CAM providers CAM can be an effective adjunct to the management of IBD CAM should be subject to strict regulations by governing health agencies Research in the efficacy and safety of CAM should be a high priority CAM interferes with the adherence to medical management of IBD When in doubt about potential drug–drug interactions of a CAM supplement, I call a pharmacist for clarification
understanding of physician practices and beliefs about CAM and how this impacts their day-to-day practice. The status of CAM in the usual medical domain remains unclear. Population-based studies have shown that patients with IBD use CAM to gain more control over their illness and disease treatment [6, 12]. It seems encouraging that respondents to our study believed that they initiate discussions on CAM at higher rates with their patients than vice versa. Increasing recognition of the importance of CAM may have resulted in a majority of gastroenterologists reporting that they were either comfortable or very comfortable discussing CAM with their patients. We believe it is important that physicians continue to discuss CAM with their patients to: (1) reassure patients that they can be actively involved in their own health care decisions; (2) assess the safety of CAM modalities; and (3) determine if any of the CAM supplements may adversely interact with traditional IBD therapies. These interactions provide an opportunity for gastroenterologists to strengthen their rapport with IBD patients by disseminating reliable sources for patient information and distilling evidence-based recommendations on CAM. Our survey results show that a relatively small number of patients are initiating discussions about CAM with their physicians. The majority of gastroenterologists believed that less than half of their patients had discussed their use of CAM as part of their treatment for IBD. Conflicting data from previous studies have presented variable findings on patient disclosure of CAM. One patient questionnaire study determined that only
Disagree (including somewhat and strongly)
Undecided
Agree (including somewhat and strongly)
15 (19)
8 (10)
55 (71)
13 (17)
12 (16)
52 (68)
18 (24)
15 (20)
43 (57)
19 (24)
17 (22)
42 (54)
13 (17) 14 (18)
12 (15) 12 (16)
26 (68) 51 (66)
5 (6)
10 (13)
61 (79)
40 (52)
15 (19)
22 (29)
26 (33)
19 (24)
19 (42)
34% of IBD patients had approached their physicians about their CAM use [7]. Similarly, in a US national survey, Eisenberg found that more than 70% of CAM users had not disclosed their practice to a physician [17]. Conversely, a survey of the Canadian IBD patients found that 71% of IBD patients had discussed CAM with their doctors, while only 13% felt uncomfortable doing so [6]. It is likely that many factors influence patient comfort level discussing CAM. Respondents to our survey suggested that a fear of disapproval was the most likely reason that patients did not mention their CAM use. Since the majority of physicians in this study believed that CAM can be an effective adjunct to IBD therapies, poor communication certainly remains a problem. A qualitative study that assessed the patient perspective of their interactions with physicians when discussing CAM also highlighted poor communication as a barrier to care. Patients in this study were concerned about physician indifference or opposition to CAM, their emphasis on scientific evidence, as well as a negative perception of CAM [18]. Despite its popularity, a lack of evidence-based data for many CAM modalities continues to hinder their acceptance into mainstream medicine. While many randomized controlled studies have attempted to test various effects of CAM on gastrointestinal disease, uncertainty remains [12, 19]. Some gastroenterologists surveyed in this study remain uncomfortable discussing CAM because of a lack of knowledge in the area. Other studies have implicated medico-legal concerns from physicians [20,
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Gallinger and Nguyen: A survey of gastroenterologists
21]. Without evidence-based recommendations and a better understanding of the physiological mechanisms of CAM therapies, physicians remain wary recommending or giving advice when questioned by their patients. This sentiment was echoed in this study whereby most respondents agreed that further research on the efficacy and safety of CAM is required. In addition, the majority of gastroenterologists believed CAM should be subject to strict regulations by health agencies. As mentioned, physician skepticism and uncertainty with respect to CAM is likely related to a lack of familiarity. Most gastroenterologists surveyed had no formal training about CAM. For physicians to gain confidence and a comfort level to instigate conversations about CAM, there may need to be more educational initiatives either during training or post-graduate CME programs that address the topic. Major organizations should also continue to offer training sessions at conferences and meetings. The results from this study confirm that gastroenterologists are aware of the various alternative therapies that are available for managing IBD. Nonetheless, the only therapy that was routinely recommended was probiotics. A number of randomized controlled trials have shown that various probiotic formulations including nonpathogenic Escherichia coli, Lactobacillus, Saccharomyces boulardii, either in combination with mesalamine, or alone, might be helpful in maintenance of remission of ulcerative colitis [18, 22, 23]. Less convincing data for the efficacy of probiotics exists for Crohn’s disease. It is also possible that aggressive marketing by the pharmaceutical industry has contributed to the widespread use of probiotics by gastroenterologists. The second most suggested form of CAM was acupuncture, with a recommendation by approximately half of gastroenterologists in our survey. This is interesting since no Level I or II evidence has shown any benefit of acupuncture in the treatment of IBD, and acupuncture is associated with risk of transmission of infectious disease by contaminated needles [24, 25]. The general popularity of acupuncture and a placebo effect may contribute to its inclusion in recommended CAM modalities by gastroenterologists. There are limitations to our study. The response rate was low but not atypical for survey-based studies. Nonetheless, it may have introduced response bias since the majority of respondents were academic physicians. Community gastroenterologists were underrepresented in our study and may offer a different perspective when treating patients with IBD. In addition, our response rate was only 10%, and of those gastroenterologists that responded, 35% had received formal training in CAM. It is possible that there may have been a selection bias toward
gastroenterologists that use CAM. Though our findings may not be representative of all American gastroenterologists, it does likely reflect attitudes of academicians, educators, and opinion leaders in the field of IBD who have influence on how the profession responds to the increasing pervasiveness of CAM. These individuals’ opinions will likely play a pivotal role in the development of educational programs and consensus recommendations regarding CAM. Though our findings may serve as an impetus for strategic initiatives related to CAM, we acknowledge the need to conduct more comprehensive surveys that encompass the opinions of community gastroenterologists. An additional limitation is the lack of a unifying definition of CAM, and thus the likelihood that the entire spectrum of CAM practices was not captured. The survey did provide an option to mention CAM modalities that we did not list. It is possible that we omitted some forms of CAM, as 16 gastroenterologists suggested additional forms of CAM that they had heard of or tried. CAM use continues to increase in popularity worldwide [15, 26]. Physicians are at the front lines when speaking with patients and will likely remain one of multiple resources for patients requesting reliable information about CAM. It is encouraging that major organization including the National Institutes of Health, University of Exeter in England, and Cochrane Collaboration have committed to providing resources to investigate and explore CAM. These initiatives will be important in equipping physicians with accurate and helpful data guide and counsel patients in CAM use. We believe our study demonstrated that gastroenterologists desire and require further training and information on CAM and hope that further qualitative studies by our group and others will help bring more insight into the patient–physician experience with IBD treatments. Acknowledgments: This study was supported by an operating grant from the Canadian Institutes of Health Research (CIHR) and the Canadian Association of Gastroenterology (CAG). G.C.N. is a recipient of New Investigator Awards by CIHR, CAG, and the Canadian Crohn’s and Colitis Foundation of Canada. Author contributions: Z.G. developed and implemented the study survey and drafted the manuscript. G.C.N. conceived and supervised the study, obtained funding, and contributed to major revisions of the manuscript. All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission. Research funding: None declared. Employment or leadership: None declared.
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Gallinger and Nguyen: A survey of gastroenterologists
Honorarium: None declared. Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.
References 1. Heuschkel R, Afzal N, Wuerth A, Zurakowski D, Leichtner A, Kemper K, et al. Complementary medicine use in children and young adults with inflammatory bowel disease. Am J Gastroenterol 2002;97:382–8. 2. Eisenberg DM, Davis RB, Ettner SL, Appel S, Wilkey S, Van Rompay M, et al. Trends in alternative medicine use in the united states, 1990-1997: results of a follow-up national survey. J Am Med Assoc 1998;280:1569–75. 3. Kessler RC, Davis RB, Foster DF, Van Rompay MI, Walters EE, Wilkey SA, et al. Long-term trends in the use of complementary and alternative medical therapies in the united states. Ann Intern Med 2001;135:262–8. 4. Limdi JK, Butcher RO. Complementary and alternative medicine use in inflammatory bowel disease. Inflamm Bowel Dis 2011;17: E86–8. 5. Joos S, Rosemann T, Szecsenyi J, Hahn EG, Willich SN, Brinkhaus B. Use of complementary and alternative medicine in Germany – a survey of patients with inflammatory bowel disease. BMC Complement Altern Med 2006;6:19. 6. Hilsden R. Complementary and alternative medicine use by Canadian patients with inflammatory bowel disease: results from a national survey. Am J Gastroenterol 2003;98:1563–8. 7. Weizman AV, Ahn E, Thanabalan R, Leung W, Croitoru K, Silverberg MS, et al. Characterisation of complementary and alternative medicine use and its impact on medication adherence in inflammatory bowel disease. Aliment Pharmacol Ther 2011;35:342–9. 8. Ganguli SC, Cawdron R, Irvine EJ. Alternative medicine use by Canadian ambulatory gastroenterology patients: secular trend or epidemic? Am J Gastroenterol 2004;99:319–26. 9. Langmead L, Rampton D. Review article: complementary and alternative therapies for inflammatory bowel disease. Aliment Pharmacol Ther 2006;23:341–9. 10. Moser G, Tillinger W, Sachs G, Maier-Dobersberger T, Wyatt J, Vogelsang H, et al. Relationship between the use of unconventional therapies and disease-related concerns: a study of patients with inflammatory bowel disease. J Psychosom Res 1996;40:503–9.
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11. Kelwala S. Why patients use alternative medicine. J Am Med Assoc 1998;280:1660–1. 12. Hilsden RJ, Verhoef MJ. Complementary and alternative medicine: evaluating its effectiveness in inflammatory bowel disease. Inflamm Bowel Dis 1998;4:318–23. 13. Barnes J. Pharmacovigilance of herbal medicines. Drug Saf 2003;26:829–51. 14. Niggemann B, Grüber C. Side-effects of complementary and alternative medicine. Allergy 2003;58:707–16. 15. Wetzel MS, Kaptchuk TJ, Haramati A, Eisenberg DM. Complementary and alternative medical therapies: implications for medical education. Ann Intern Med 2003;138:191–6. 16. Hilsden RJ, Verhoef MJ, Rasmussen H, Porcino A, DeBruyn JC. Use of complementary and alternative medicine by patients with inflammatory bowel disease. Inflamm Bowel Dis 2011;17:655–62. 17. Eisenberg DM, Kessler RC, Foster C, Norlock FE, Calkins DR, Delbanco TL. Unconventional medicine in the United States. Prevalence, costs, and patterns of use. N Engl J Med 1993;328:246–52. 18. Tasaki K, Maskarinec G, Shumay DM, Tatsumura Y, Kakai H. Communication between physicians and cancer patients about complementary and alternative medicine: exploring patients’ perspectives. Psychooncology 2002;11:212–20. 19. Koretz RL, Rotblatt M. Complementary and alternative medicine in gastroenterology: the good, the bad, and the ugly. Clin Gastroenterol Hepatol 2004;2:957–67. 20. Golnik AE, Ireland M. Complementary therapy medicine for children with autism: a physician survey. J Autism Dev Disord 2009;39:996–1005. 21. O’Beirne M, Verhoef M, Paluck E, Herbert C. Complementary therapy use by cancer patients. Physicians’ perceptions, attitudes, and ideas. Can Fam Physician 2004;50:882–8. 22. Shanahan F. Probiotics and inflammatory bowel disease: is there a scientific rationale? Inflamm Bowel Dis 2000;6:107–15. 23. Kruis W. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 2004;53:1617–23. 24. Durber J, Otley A. Complementary and alternative medicine in inflammatory bowel disease: keeping an open mind. Expert Rev Clin Immunol 2005;1:277–92. 25. Ernst E, Sherman KJ. Is acupuncture a risk factor for hepatitis? Systematic review of epidemiological studies. J Gastroenterol Hepatol 2003;18:1231–6. 26. Maha N, Shaw A. Academic doctors’ views of complementary and alternative medicine (CAM) and its role within the NHS: an exploratory qualitative study. BMC Complement Altern Med 2007;7:17.
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Zane R. Gallinger and Geoffrey C. Nguyen*
Practices and attitudes toward complementary and alternative medicine in inflammatory bowel disease: a survey of gastroenterologists Abstract Background: Use of complementary and alternative medicine (CAM) is increasingly prevalent among patients with inflammatory bowel disease (IBD). We sought to characterize the practices and attitudes of IBD physician providers toward CAM. Methods: A web-based survey was sent to non-trainee physician members of the American Gastroenterological Association with an interest in IBD. The survey included multiple-choice and Likert scale questions which queried physician perceptions of CAM and their willingness to discuss CAM with patients. Results: The vast majority of respondents (80%) considered themselves IBD subspecialists with 75% holding academic appointments. Nearly a third reported initiating conversations on CAM in the majority of their patient interactions, while 90% perceived that a majority of their patients were reluctant to bring up the topic of CAM. Nearly three quarters (72%) of respondents felt comfortable discussing CAM, while those that did not most frequently cited lack of knowledge as the reason. More than half (55%) stated they had no systematic approach to discussing CAM. Most gastroenterologists (65%) reported no formal training in CAM. Most gastroenterologists had recommended use of probiotics, and nearly half had recommended acupuncture. A vast majority believed that there was adjunctive role for CAM in treatment of IBD. Conclusions: Academic IBD specialists were receptive to the use of CAM, and most felt that it had a role in the treatment of IBD, without necessarily compromising conventional therapy. Formal educational initiatives and societal recommendations on the use of CAM may facilitate a more systematic approach to its use in daily practice. *Corresponding author: Geoffrey C. Nguyen, Mount Sinai Hospital Centre for Inflammatory Bowel Disease, University of Toronto, Toronto, ON, Canada; University of Toronto, Department of Medicine, Toronto ON, Canada, E-mail: [email protected] Zane R. Gallinger, University of Toronto, Department of Medicine, Toronto ON, Canada
Keywords: complementary and alternative medicine, Crohn’s disease, inflammatory bowel disease, ulcerative colitis DOI 10.1515/jcim-2014-0008 Received February 16, 2014; accepted August 29, 2014; previously published online October 7, 2014
Introduction The use of complementary and alternative medicine (CAM) has risen steadily across many countries over the past few decades [1–5]. While once considered an unconventional modality, CAM is now a multibillion-dollar industry. The National Center for Complementary and Alternative Medicine, a part of the National Institute of Health (NIH), reported that Americans spent nearly $34 billion on CAM in 2008 alone. Originally a therapy considered popular only among fringe demographics, the characteristics of individuals who use CAM appear to be narrowing [6]. Nonetheless, patients with specific diseases continue to use CAM more than others [7, 8]. One group known to use CAM at higher rates than the general population are those with inflammatory bowel disease (IBD), with some studies showing that nearly half of all IBD populations have used CAM [5, 6, 9]. The generally chronic course of IBD, the lack of consistently effective traditional therapies, as well as patients desire to gain control over their illness, are reasons that some have suggested IBD patients use CAM at high rates [10, 11]. Multiple educational resources exist for patients to access information on CAM, however it remains unclear if patients consider their physicians a reliable resource for information on CAM [12]. As CAM use rises, it can be expected that physicians will be increasingly relied upon to provide information to patients that seek advice on this treatment modality. Physicians have, however, been reluctant to engage in this topic because of lack of clinical trial data and government regulation [13]. Moreover, adverse interactions between CAM and conventional therapies prescribed by physicians have been described [14]. The above concerns
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298
Gallinger and Nguyen: A survey of gastroenterologists
may lead to uncertainty about CAM, and subsequently poor communication with patients. Nonetheless, the number of medical schools in the United States that have incorporated CAM-related medical education in their curriculum rose from 46 in 1996–1997 to 82 in 1999–2000 [15]. Given its increasing popularity, in addition to a new focus from medical schools, CAM will likely remain a relevant component of the physician–patient relationship. An understanding of physician’s perceptions of CAM and how they interact with their patients during conversations on this topic are critical in developing CAM-related educational initiatives. The purpose of this study was to examine factors that influence the relationship between gastroenterologists and patients when CAM is discussed and to assess areas of CAM that gastroenterologists feel require further focus. The results will help inform which elements of CAM require increased attention by academic and professional institutions.
Methods
questionnaire consisted of 3 screening questions for eligibility and an additional 15 questions with binary and scaled answers. A combination of contingency, matrix, and close-ended questions is used. Participants were also asked to select on a 7-point Likert scale their level of agreement or disagreement among a series of statements querying their perceptions of and practices related to CAM.
Survey administration and data collection An invitation to participate in the survey was sent to all members of the AGA who were affiliated with the Immunology, Microbiology, and IBD section. The questionnaire was administered using an online survey engine (Novi-Survey). Five separate e-mails were sent to non-responders after the initial invitation in 1-month intervals. Participants who selected the link to the survey site were given an explanation of the study, and consent was implied if participants proceeded to the survey. All respondents were anonymously assigned a unique identifier, and table and graphs were created using Microsoft Excel.
Study population Ethics approval All gastroenterologists who were members of the American Gastroenterological Association (AGA), and were affiliated with the IBD sub-section, were invited to participate. Additional inclusion criteria included being a practicing physician having cared for IBD patients in the prior 12 months and having had completed medical, specialty, and/or subspecialty training.
The study protocol was approved by the Research Ethics Board at Mount Sinai Hospital, Toronto, Ontario.
Results Study population
Study design and content We distributed a questionnaire to gastroenterologists to assess their opinions and practices toward patients who use CAM. The questionnaire was reviewed and critiqued by IBD specialists to increase its face validity. Although there is no universally accepted definition of CAM, the National Center for Complementary and Alternative Medicine broadly defines it as “diverse medical and healthcare systems, practices, and products not considered as conventional medicine” [16]. In our survey, CAM referred to agents, which included, but were not limited to meditation, acupuncture, traditional Chinese medicine, probiotics, massage, and herbal diets. The
There were 95 respondents to the survey which translated into an approximately 10% response rate. A total of 78 of respondents met inclusion criteria. Three quarters of respondents practiced in an academic setting or had an academic appointment. The mean length of time in practice was 17 years (standard deviation (SD), 12.5 years; Table 1). The majority of respondents (80%) considered themselves IBD subspecialists. However, 60% reported having less than 50% of their practice comprised IBD patients. The vast majority of respondents (80%) suggested that adult gastroenterology (GI) was their primary practice, while 17% practiced pediatric GI (Table 1).
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Gallinger and Nguyen: A survey of gastroenterologists
Table 1
Practice characteristics of respondents n (%).
Years in practice, mean SD
17.4 12.5
Primary practice setting Academic Community Both Scope of practice Limited to adult gastroenterology Gastroenterology and internal medicine Pediatric gastroenterology Surgery Other Percentage of gastroenterology practice patients with IBD < 10 10–25 25–50 > 50 Considered self-subspecialist in IBD Yes No
49 (63) 20 (26) 9 (12) 62 (79) 2 (2) 13 (17) 0 (0) 1 (1)
16 (20) 24 (31) 10 (13) 28 (36) 62 (80) 16 (20)
Patient–physician interactions related to CAM When queried about interactions with their patients on the topic of CAM, approximately one third (29%) of respondents reported that they independently initiated a discussion on CAM with over half of their patient population. A vast majority of gastroenterologists (90%) reported that less than half of their patient population initiated a discussion on CAM. Similarly, a minority of (14%) gastroenterologists believed that more than one half of their patients had mentioned their use of CAM as part of treatment for their IBD. Only 12% of gastroenterologists believed that a majority of their patients use CAM without keeping their physicians informed (Table 2). Sixty-eight percent of
Table 2
physicians believed their potential disapproval was the reason patients withheld information on their use of CAM.
Comfort level and CAM Nearly three quarters of respondents (72%) felt comfortable or very comfortable discussing CAM with their patients (Figure 1A). The most common reasons for discomfort with discussing CAM were lack of knowledge and the belief that it was not useful (Figure 1B). The majority of gastroenterologists (65%) had never received any formal training about CAM. Just over a third of gastroenterologists reported training in CAM with the majority gaining exposure through continued medical education sessions (55%) while other received training through independent learning (22%), medical school (15%), and hospital workshops (7%). Over half of gastroenterologists (55%) acknowledged that their response to patient CAM use varied from individual to individual. An additional 30% reported that they are willing to participate in the initial discussion about CAM with their patients, while 10% actively recommend CAM once their patients have engaged them in conversation. No gastroenterologists dismissed CAM outright, and one was willing to refer their patients to an alternative practitioner.
Types of CAM The majority of gastroenterologists had heard of the various forms of CAM listed (Figure 2), with the exception of wormwood, Boswellia serrata, and Andrographis paniculata. Figure 2 shows the forms of CAM recommended by gastroenterologists with probiotics (86%) and acupuncture (47%) being the most commonly cited (Figure 2).
Responses to specific questions surrounding interactions with patients and CAM use n (%).
What percentage of your patients has mentioned the use of CAM as a part of their treatment of IBD? How often do you initiate a discussion with your patients about their use of CAM? How often does a patient with IBD initiate a discussion about their use of CAM? What percentage of your patients do you think use CAM and do not tell you about it?
299
< 10%
10–25%
25–50%
21 (27)
27 (35)
19 (24)
11 (14)
19 (24)
19 (24)
17 (19)
23 (29)
19 (25)
30 (39)
20 (26)
8 (10)
23 (29)
24 (31)
22 (28)
9 (12)
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> 50%
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Gallinger and Nguyen: A survey of gastroenterologists
Figure 1 Comfort levels and CAM. (A) Comfort levels of gastroenterologists when discussing CAM with their patients. (B) Reason that respondents were not comfortable or only somewhat comfortable discussing CAM with patients.
Figure 2 Gastroenterologists’ familiarity with and recommendation practices for specific modalities of CAM. Black bars the proportion of respondents who were familiar with a specific type of CAM and gray bars represent the proportion who recommended that specific modality.
Gastroenterologist beliefs about CAM Table 3 displays responses by gastroenterologists about their beliefs and attitudes toward CAM. The majority believed that their patients would pursue CAM despite their recommendations for or against it. Respondents felt there needed to be more regulatory oversight of CAM and more studies to demonstrate its efficacy. Most gastroenterologists believed that patients who responded poorly to conventional IBD medical therapy most often used CAM. Half of the physicians surveyed did not believe that CAM would interfere with adherence to medical management of IBD, while 20% were not sure. A vast
majority of respondents believed that CAM could play an important adjunctive role in the treatment of IBD.
Discussion This survey study described the approach and beliefs of American gastroenterologists toward CAM and how these attitudes influenced their interactions with patients that use CAM to treat IBD. As the popularity and use of CAM increase, physicians will continue to be tasked with the responsibility of discussing merits and drawbacks of CAM with their patients. We believe it is important to gain an
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Gallinger and Nguyen: A survey of gastroenterologists
Table 3
301
Perceptions of CAM efficacy, user characteristics, and utility in patients that use it to treat IBD n (%).
Patients who have poor response to conventional IBD therapy tend to use more CAM My patients will pursue CAM despite my recommendations for or against it Women, high income, and high education patients are more likely to use CAM My patients would benefit from a wellness center at my institution that could provide access to CAM providers CAM can be an effective adjunct to the management of IBD CAM should be subject to strict regulations by governing health agencies Research in the efficacy and safety of CAM should be a high priority CAM interferes with the adherence to medical management of IBD When in doubt about potential drug–drug interactions of a CAM supplement, I call a pharmacist for clarification
understanding of physician practices and beliefs about CAM and how this impacts their day-to-day practice. The status of CAM in the usual medical domain remains unclear. Population-based studies have shown that patients with IBD use CAM to gain more control over their illness and disease treatment [6, 12]. It seems encouraging that respondents to our study believed that they initiate discussions on CAM at higher rates with their patients than vice versa. Increasing recognition of the importance of CAM may have resulted in a majority of gastroenterologists reporting that they were either comfortable or very comfortable discussing CAM with their patients. We believe it is important that physicians continue to discuss CAM with their patients to: (1) reassure patients that they can be actively involved in their own health care decisions; (2) assess the safety of CAM modalities; and (3) determine if any of the CAM supplements may adversely interact with traditional IBD therapies. These interactions provide an opportunity for gastroenterologists to strengthen their rapport with IBD patients by disseminating reliable sources for patient information and distilling evidence-based recommendations on CAM. Our survey results show that a relatively small number of patients are initiating discussions about CAM with their physicians. The majority of gastroenterologists believed that less than half of their patients had discussed their use of CAM as part of their treatment for IBD. Conflicting data from previous studies have presented variable findings on patient disclosure of CAM. One patient questionnaire study determined that only
Disagree (including somewhat and strongly)
Undecided
Agree (including somewhat and strongly)
15 (19)
8 (10)
55 (71)
13 (17)
12 (16)
52 (68)
18 (24)
15 (20)
43 (57)
19 (24)
17 (22)
42 (54)
13 (17) 14 (18)
12 (15) 12 (16)
26 (68) 51 (66)
5 (6)
10 (13)
61 (79)
40 (52)
15 (19)
22 (29)
26 (33)
19 (24)
19 (42)
34% of IBD patients had approached their physicians about their CAM use [7]. Similarly, in a US national survey, Eisenberg found that more than 70% of CAM users had not disclosed their practice to a physician [17]. Conversely, a survey of the Canadian IBD patients found that 71% of IBD patients had discussed CAM with their doctors, while only 13% felt uncomfortable doing so [6]. It is likely that many factors influence patient comfort level discussing CAM. Respondents to our survey suggested that a fear of disapproval was the most likely reason that patients did not mention their CAM use. Since the majority of physicians in this study believed that CAM can be an effective adjunct to IBD therapies, poor communication certainly remains a problem. A qualitative study that assessed the patient perspective of their interactions with physicians when discussing CAM also highlighted poor communication as a barrier to care. Patients in this study were concerned about physician indifference or opposition to CAM, their emphasis on scientific evidence, as well as a negative perception of CAM [18]. Despite its popularity, a lack of evidence-based data for many CAM modalities continues to hinder their acceptance into mainstream medicine. While many randomized controlled studies have attempted to test various effects of CAM on gastrointestinal disease, uncertainty remains [12, 19]. Some gastroenterologists surveyed in this study remain uncomfortable discussing CAM because of a lack of knowledge in the area. Other studies have implicated medico-legal concerns from physicians [20,
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Gallinger and Nguyen: A survey of gastroenterologists
21]. Without evidence-based recommendations and a better understanding of the physiological mechanisms of CAM therapies, physicians remain wary recommending or giving advice when questioned by their patients. This sentiment was echoed in this study whereby most respondents agreed that further research on the efficacy and safety of CAM is required. In addition, the majority of gastroenterologists believed CAM should be subject to strict regulations by health agencies. As mentioned, physician skepticism and uncertainty with respect to CAM is likely related to a lack of familiarity. Most gastroenterologists surveyed had no formal training about CAM. For physicians to gain confidence and a comfort level to instigate conversations about CAM, there may need to be more educational initiatives either during training or post-graduate CME programs that address the topic. Major organizations should also continue to offer training sessions at conferences and meetings. The results from this study confirm that gastroenterologists are aware of the various alternative therapies that are available for managing IBD. Nonetheless, the only therapy that was routinely recommended was probiotics. A number of randomized controlled trials have shown that various probiotic formulations including nonpathogenic Escherichia coli, Lactobacillus, Saccharomyces boulardii, either in combination with mesalamine, or alone, might be helpful in maintenance of remission of ulcerative colitis [18, 22, 23]. Less convincing data for the efficacy of probiotics exists for Crohn’s disease. It is also possible that aggressive marketing by the pharmaceutical industry has contributed to the widespread use of probiotics by gastroenterologists. The second most suggested form of CAM was acupuncture, with a recommendation by approximately half of gastroenterologists in our survey. This is interesting since no Level I or II evidence has shown any benefit of acupuncture in the treatment of IBD, and acupuncture is associated with risk of transmission of infectious disease by contaminated needles [24, 25]. The general popularity of acupuncture and a placebo effect may contribute to its inclusion in recommended CAM modalities by gastroenterologists. There are limitations to our study. The response rate was low but not atypical for survey-based studies. Nonetheless, it may have introduced response bias since the majority of respondents were academic physicians. Community gastroenterologists were underrepresented in our study and may offer a different perspective when treating patients with IBD. In addition, our response rate was only 10%, and of those gastroenterologists that responded, 35% had received formal training in CAM. It is possible that there may have been a selection bias toward
gastroenterologists that use CAM. Though our findings may not be representative of all American gastroenterologists, it does likely reflect attitudes of academicians, educators, and opinion leaders in the field of IBD who have influence on how the profession responds to the increasing pervasiveness of CAM. These individuals’ opinions will likely play a pivotal role in the development of educational programs and consensus recommendations regarding CAM. Though our findings may serve as an impetus for strategic initiatives related to CAM, we acknowledge the need to conduct more comprehensive surveys that encompass the opinions of community gastroenterologists. An additional limitation is the lack of a unifying definition of CAM, and thus the likelihood that the entire spectrum of CAM practices was not captured. The survey did provide an option to mention CAM modalities that we did not list. It is possible that we omitted some forms of CAM, as 16 gastroenterologists suggested additional forms of CAM that they had heard of or tried. CAM use continues to increase in popularity worldwide [15, 26]. Physicians are at the front lines when speaking with patients and will likely remain one of multiple resources for patients requesting reliable information about CAM. It is encouraging that major organization including the National Institutes of Health, University of Exeter in England, and Cochrane Collaboration have committed to providing resources to investigate and explore CAM. These initiatives will be important in equipping physicians with accurate and helpful data guide and counsel patients in CAM use. We believe our study demonstrated that gastroenterologists desire and require further training and information on CAM and hope that further qualitative studies by our group and others will help bring more insight into the patient–physician experience with IBD treatments. Acknowledgments: This study was supported by an operating grant from the Canadian Institutes of Health Research (CIHR) and the Canadian Association of Gastroenterology (CAG). G.C.N. is a recipient of New Investigator Awards by CIHR, CAG, and the Canadian Crohn’s and Colitis Foundation of Canada. Author contributions: Z.G. developed and implemented the study survey and drafted the manuscript. G.C.N. conceived and supervised the study, obtained funding, and contributed to major revisions of the manuscript. All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission. Research funding: None declared. Employment or leadership: None declared.
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Gallinger and Nguyen: A survey of gastroenterologists
Honorarium: None declared. Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.
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