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Journal of Clinical Oncology, Vol 25, No 36 (December 20), 2007: pp. 5748-5752
© 2007 American Society of Clinical Oncology.
DOI: 10.1200/JCO.2007.12.4180

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Oncologist Communication About Emotion During Visits With Patients With Advanced Cancer

Kathryn I. Pollak, Robert M. Arnold, Amy S. Jeffreys, Stewart C. Alexander, Maren K. Olsen, Amy P. Abernethy, Celette Sugg Skinner, Keri L. Rodriguez, James A. Tulsky

From the Duke Comprehensive Cancer Center, Cancer Prevention, Detection, and Control Research Program; the Department of Community and Family Medicine; the Department of Biostatistics and Bioinformatics; the Department of Medicine; the Center for Palliative Care, Duke University Medical Center; the Center for Health Services Research, Durham Veterans Affairs Medical Center, Durham, NC; the Division of General Internal Medicine, Department of Medicine; the Institute for Doctor-Patient Communication; the Institute to Enhance Palliative Care, University of Pittsburgh School of Medicine; and the Veterans Affairs Pittsburgh Healthcare System, Pittsburgh, PA

Address reprint requests to Kathryn I. Pollak, PhD, Duke University Medical Center, Community and Family Medicine, 2424 Erwin Rd, Suite 602, Durham, NC 27705; e-mail: polla007{at}mc.duke.edu


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 Author Contributions
 REFERENCES
 
Introduction: Cancer care involves addressing patient emotion. When patients express negative emotions, empathic opportunities emerge. When oncologists respond with a continuer statement, which is one that offers empathy and allows patients to continue expressing emotions, rather than with a terminator statement, which is one that discourages disclosure, patients have less anxiety and depression and report greater satisfaction and adherence to therapy. We studied whether oncologist traits were associated with empathic opportunities and empathic responses.

Patients and Methods: We audio-recorded 398 clinic conversations between 51 oncologists and 270 patients with advanced cancer; oncologists also completed surveys. Conversations were coded for the presence of empathic opportunities and oncologist responses. Analyses examined the relationship with oncologists' demographics, self-reported confidence, outcome expectancies, and comfort to address social versus technical aspects of care.

Results: In 398 conversations, 37% contained at least one empathic opportunity; the range was 0 to 10, and the total empathic opportunities was 292. When they occurred, oncologists responded with continuers 22% of the time. Oncologist sex was related to the number of empathic opportunities; female patients seen by female oncologists had the most empathic opportunities (P = .03). Younger oncologists (P = .02) and those who rated their orientation as more socioemotional than technical (P = .03) were more likely to respond with empathic statements.

Conclusion: Oncologists encountered few empathic opportunities and responded with empathic statements infrequently. Empathic responses were more prevalent among younger oncologists and among those who were self-rated as socioemotional. To reduce patient anxiety and increase patient satisfaction and adherence, oncologists may need training to encourage patients to express emotions and to respond empathically to patients' emotions.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 Author Contributions
 REFERENCES
 
High-quality cancer care relies on effective patient-oncologist communication, particularly among patients with advanced cancer whose emotional suffering may be quite intense. Such suffering often manifests as anxiety and depression,1 and when patients are able to disclose their concerns fully, they may cope better.2,3 Yet, patients with cancer typically disclose only 50% of their emotional concerns to oncologists.4,5 Patients may not want to burden oncologists with their concerns and instead may provide indirect cues or clues about their concerns.6 For example, rather than ask about prognosis, patients may simply say, "I'm not sure what there is to look forward to. " These indirect cues are often missed by oncologists.1,7-9

Such cues or clues often create empathic opportunities, or moments that beg empathic responses from clinicians.10 Empathic responses directly address patients' emotions, validate their feelings, and invite further disclosure. Such responses are considered empathic continuers. Unfortunately, clinicians often do not respond to cues with expressions of empathy. They may avoid the emotion or may change the topic with empathic terminators that can negatively affect the patient-physician relationship. In response, some patients do not express any further emotions. Others continue to express emotion until their providers respond; this re-expression of emotion can increase visit time. Empathic continuers strengthen the patient-physician relationship, increase patient satisfaction, decrease the need to restate the negative emotion, and may make patients more likely to disclose future concerns.11,12 In addition, when oncologists respond empathically, patients are more likely to adhere to treatment plans.13 No researchers have examined how oncologist factors influence their elicitation of and response to patient emotion.

To assess the prevalence and nature of empathic communication in cancer care, we analyzed audio-recorded patient-oncologist outpatient visits. We examined oncologist factors that influence whether empathic opportunities arise and how oncologists respond in visits with patients with advanced cancer.


    PATIENTS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 Author Contributions
 REFERENCES
 
Participants
This report presents data from the Studying Communication in Oncologist-Patient Encounters (SCOPE) project, a three-site study from Duke University, the Durham Veterans Affairs Medical Center, and the University of Pittsburgh. This report included 398 audio-recorded conversations between 51 oncologists and 270 patients with advanced cancer. Fifty-three percent of patients had one visit audio-recorded; the other 47% had two visits with the same oncologist audio-recorded. Details of the study are reported elsewhere.14

Oncologists
We approached 110 medical, gynecologic, and radiation oncologists to participate in the study. Of the 110 oncologists, 74 (67%) consented. Twenty-one (19%) were ineligible because they did not see enough patients, and 15 (14%) refused. Of the 74 who consented, 51 had enough audio recordings (at least six) to include in this sample. A faculty investigator met with each oncologist to introduce the study. If oncologists agreed to participate, they signed a consent form and completed a baseline survey. Participating oncologists were offered $25 gift certificates on completion of the audio recordings of their visits.

Patients
Our goal was to identify patients with sufficiently advanced disease to increase the probability that conversations would contain emotional concerns. We asked oncologists or their midlevel provider staff to identify patients of whom they would not be surprised by death within 1 year. We assured oncologists and providers that this information would not be conveyed to patients. Patients provided written informed consent to participate and were told they were asked to enroll because they had been diagnosed with cancer. Other eligibility criteria included that patients spoke English; received primary oncology care at one of our study sites; and had access to a telephone.

Identified patients were sent an introductory letter and brochure that included a toll-free number that they could call to refuse participation. Patients who did not call within 10 days were contacted by phone. At this time, interviewers described the study to patients and asked permission to approach them in the clinic before their next scheduled oncology visit. Patients received a free parking pass ($7 value [US $]) for each visit that was recorded. Patients were ineligible if they were unable to provide informed consent as assessed by the interviewer (eg, dementia, delirium, or mental illness); were seen primarily by nonphysician providers or medical residents; were hearing impaired; or had a speech disorder.

Audio Recordings
Every attempt was made to audio-record conversations in oncology clinics without disrupting clinic flow. We contacted oncologists with reminders 1 day before the designated visit. We placed digital recorders unobtrusively in the exam rooms before the oncologists entered and retrieved recorders at the end of the visit. We asked all health care providers and family members present to sign a consent form that allowed their voiced to be audio-recorded. This protocol was approved by each institution's institutional review board.

We used Suchman's definitions of empathic opportunities and physicians' responses to them.10 These definitions are based solely on patients' verbal expressions of negative emotions, not on positive emotions or praise opportunities. Two independent coders were trained extensively; 15% of audio recordings were coded by both raters. Interrater reliability was high for the presence of an empathic opportunity ({kappa} = 0.71). We coded whether patients expressed the emotion directly or indirectly. Some indirect empathic opportunities relied on tone or pace of voice (eg, "Well... I guess it is what it is"). We coded physicians' responses as empathic continuers or terminators ({kappa} = 0.71) Table 1 lists example codes and {kappa} measures. Continuers consisted of five behaviors that have been organized by educators under the mnemonic NURSE: Name, Understand, Respect, Support, and Explore.15-17


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Table 1. Codes for Empathic Opportunities and for NURSE Continuers

 
Survey Measures
Physicians completed a baseline survey before the audio recording. We assessed factors that might be related to the presence of and response to empathic opportunities.18 Some factors are based on social cognitive theory19 and may affect whether physicians create environments in which patients feel comfortable expressing emotions and how oncologists respond when patients express emotions. Oncologists may lack the confidence to address emotion.20 Oncologists also may have low outcome expectancies that addressing emotion will lead to better outcomes.21 Finally, oncologists may see themselves as more technical rather than socioemotional in orientation and therefore may be more comfortable addressing medical rather than psychosocial issues.22

Physician demographics. At baseline, oncologists were asked to report their age, race, ethnicity, sex, and years in practice.

Confidence. Oncologists were asked seven items about their confidence in addressing patients' concerns. Sample items read, "Please rate how successful you think you would be in...'initiating a discussion about a patient's concerns, ' and ‘moving patient to discuss other concerns’" (1 = not at all confident to 5 = extremely confident; {alpha} = .92).23

Outcome expectancies. Oncologists were asked an adapted nine-item communication outcomes questionnaire to assess possible outcomes of communication behaviors. A sample item read, "Your patient will become uncontrollably upset if you ask about his or her feelings" (1 = not unlikely to 5 = very likely). We reversed the metric to make positive outcome expectancies higher scores. In our sample, this scale had moderate reliability of {alpha} = .61, unlike the higher reliability reported in another study.21

Comfort with psychosocial talk. Oncologists were asked the Physician Belief Scale, which includes 32 items to assess comfort with psychosocial talk. A sample item read, "Doctors should not focus on psychosocial problems until they have ruled out organic disease " (1 = strongly agree to 5 = strongly disagree; {alpha} = .84; summed score ranged from 32 to 160).24

Socioemotional versus technical orientation. Oncologists answered two questions to assess their socioemotional orientation. The questions read, "Do you think you are more inclined toward the social and emotional aspects of patient care or more inclined toward the technological and scientific aspects? " (social and emotional v technological and scientific) and, "Are you a little more inclined to the aspects you chose in the last question or a lot more inclined? " (a little more inclined v a lot more inclined).22

Analyses
Our primary dependent variables were the number of empathic opportunities and empathic continuer responses. The number of empathic opportunities was coded for each conversation and then was summed for each oncologist. Wilcoxon rank sum tests and Pearson correlation coefficients were used to examine the relationship between the number of empathic opportunities and oncologist factors. For each oncologist, we calculated the number of empathic opportunities in which he or she responded with a continuer. We then dichotomized this variable: oncologists who never used a continuer versus oncologists who used at least one continuer. {chi}2 tests, t tests, and Wilcoxon rank sum tests were used to examine the relationship between continuers and oncologist factors. Analyses were conducted using SAS Version 9.2 (SAS Institute Inc, Cary, NC).


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 Author Contributions
 REFERENCES
 
Sample Demographics
Fifty-one oncologists participated; most were white and male (Table 2); mean age was 44.7 years (standard deviation [SD], 8.4 years); most were medical oncologists (90%), whereas others were gynecological oncologists (8%) and radiation oncologists (2%). Of the 270 patients, 74% were white, 50% were male, and the mean age was 60.4 years (SD, 12.9). Malignancies represented were hematologic (28%), lung (16%), breast (15%), colon or gastrointestinal (12%), brain (10%), and other (19%), which included gynecologic, prostate, and head and neck. According to physician post-visit surveys, 70% of the patients were currently undergoing treatment, and 74% of these were receiving chemotherapy. Most patients were not new patients to the oncologists; 90% had known their oncologists for at least 6 months and had more than two visits. The mean length of conversations was 18 minutes (SD, 14; range, 0.5 to 88 minutes).


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Table 2. Demographics of Patients and Physicians

 
Oncologists reported high confidence in their abilities to address patients' concerns (mean, 4.0; SD, 0.6 on a 5-point scale) and moderate beliefs that addressing emotions would benefit patients (mean, 3.9; SD, 0.4 on a 5-point scale). Most reported being somewhat comfortable with psychosocial talk (mean, 84.5; SD, 9.9 on a 0 to 100 scale) and were more likely to rate their orientation as technical (67%) than socioemotional. Sixty-one percent of oncologists stated that they had received some past communication training.

Empathic Opportunities
A total of 292 empathic opportunities occurred in 398 conversations (mean, 0.73; SD, 1.34; range, 0 to 10 per conversation). Across all conversations (range, 6 to 8 conversations per oncologist), oncologists encountered a median of 5.0 empathic opportunities each (interquartile range = 6.0), with one oncologist encountering none and 17 (one third of total) having three or fewer. Of the 292 empathic opportunities, 68% were direct and 33% were indirect. An example of a direct empathic opportunity was, "I'm scared about what my lower white blood count means. " An example of an indirect empathic opportunity was, "Oh no. What do we do now? " Forty-seven percent of patients expressed an empathic opportunity at some point in all of their recorded conversations. Conversations shorter than 10 minutes were less likely to contain an empathic opportunity than conversations lasting 10 minutes or more (P < .0001).

Responses to Empathic Opportunities
When patients initiated an empathic opportunity, oncologists responded with continuers in 27% of patient cases and terminators 73% of the time. An example continuer was, "It's not easy for anybody in your family. " An example terminator was, "Give us time. We are getting there," which represents premature reassurance for a patient who was feeling upset at his progress. Forty-one percent of oncologists never used a continuer in response to an empathic opportunity. There was no difference in response based on whether patients expressed their emotions directly or indirectly.

Oncologist Characteristics, Empathic Opportunities, and Responses
Presence of empathic opportunities was related to sex concordance of the patient and the oncologist (P = .03). The percentage of visits containing at least one empathic opportunity were as follows: 52% of those in which female patients saw female oncologists; 44% in which female patients saw male oncologists; and 28% of male patients' visits with either sex of the oncologist. No other variables were associated with the presence of empathic opportunities.

Several oncologist characteristics were related to their responses to empathic opportunities (Table 3). Oncologists who used more empathic statements were younger than those who did not (mean age of those who used at least one continuer, 42.4 years; SD, 7.8; mean age of those who never used a continuer, 48.1 years; SD, 8.3; P = .02). Also, oncologists who responded with at least one continuer were more likely to describe themselves as socioemotional rather than technical (80% v 45% for socioemotional and technical, respectively; P = .03). No other variables were associated with responses to empathic opportunities, including having had communication training in the past. We do not present a multivariable model because age, sex, and socioemotional rating are related to each other in our study. Female physicians are on average 10 years younger than male physicians and are more likely to have socioemotional orientation (66.7% v 33.3%). Thus, all three variables are representing the same group: young, female oncologists who describe themselves as socioemotional.


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Table 3. Associations of Physician Attributes and Responses to Empathic Opportunities

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 Author Contributions
 REFERENCES
 
We observed nearly 400 conversations between oncologists and patients with advanced cancer and found several key results. First, empathic opportunities were relatively uncommon in these conversations; sex concordance was related to the presence of empathic opportunities. Second, oncologists generally expressed high levels of confidence, yet neither this nor previous training in communication was related to empathic opportunities or their responses. Third, and most important, empathic responses were rare. Oncologists who were younger or who rated themselves as socioemotional were most likely to respond empathically.

Empathic opportunities were not prevalent in these encounters, were less common than that found in a previous study,25 and were less frequent than those found in a study of primary care and surgery (52% and 53%, respectively).26 The low occurrence of empathic opportunities may be partially due to the types of visits that were audio-recorded. Some visits were relatively short; shorter visits were less likely to contain empathic opportunities. Although our inclusion criteria and coding did not allow us to characterize the goals of each visit, it is likely that these shorter visits were follow-up appointments for patients receiving active treatment. In such brief encounters, opportunities for patients to express emotions may have been somewhat limited. In addition, some of these patients had already been seen by fellows or midlevel providers (eg, nurse practitioners or physician assistants), which left the physician visit as a brief opportunity for the patient and oncologist to check in with each other. This is a relatively common practice in our oncology clinics and may differ from oncology care in other countries, such as Australia and the United Kingdom. It also could be that, because oncologists did not respond to patient emotion with empathic continuers, the patients were less likely to express other emotions.

Female patients were more likely to raise at least one negative emotion, and thus create an empathic opportunity, when their oncologist was a woman. Although many have examined sex differences in communication in general,27 no one has examined how sex concordance affects patients' expression of emotion. Women are more comfortable discussing emotions than men.28 Therefore, it may be that, when both members of the dyad are women, patients are more comfortable expressing their emotions. No other factors were associated with patient expression of negative emotion.

Further, we found that oncologists were confident that they could address patient emotion and also that they perceived that addressing emotion would help patients or themselves. With moderate to high levels of confidence and outcome expectancies, it is not surprising that neither was related to the presence of or response to empathic opportunities. For these important constructs, better measures with more variability are needed. For other physician skills, confidence and outcome expectancies are predictors.29 It may be that oncologists are confident they can address patient emotion, but they are not confident they can recognize patient emotion when it occurs. We did not differentiate between confidences for these different skills.

Finally, on average, oncologists responded to patient emotion with empathic language only 22% of the time. Although limited time may curtail one's ability to explore emotional content, it should not affect the oncologist's ability to respond with at least a brief empathic statement when negative emotions are expressed. When oncologists do not do so, they risk increasing patient distress.11,12

Some oncologists were more likely to respond to patient emotion with empathic language. The prevalence of this behavior among younger oncologists could reflect more recent shifts in training that has focused on patient-physician communication. Younger physicians in this study received their training in the early 1990s, when physician-patient communication skills were already commonly taught in medical schools and residencies. However, even though more than half of oncologists stated that they had received previous communication training, training was unrelated to responses to empathic opportunities. Alternatively, younger oncologists may be less likely to have experienced burnout from the challenging field of cancer care and may still attend to the subtle signals patients send. Oncologists who self-rated as more socioemotional were more likely to use continuers in response to empathic opportunities. It is unknown what contributes to an oncologist feeling more comfortable with socioemotional factors than technical factors. Indeed, most oncologists participating in our study rated themselves as more technical than socioemotional, which differs greatly from physicians who choose to enter primary care fields.30 It may be that oncologists who are more socioemotionally oriented entered oncology for different reasons than those who view themselves as more technical. Further, it is unknown whether this trait is modifiable through intervention.

This study has several limitations. First, oncologists were not asked to choose conversations expected to be emotionally-laden (eg, delivering bad news). Therefore, the low prevalence of empathic opportunities may result from the types of visits audio-recorded. We could not differentiate among the types of visits in our analyses. Second, most oncologists who participated in this study came from academic medical centers; this may limit generalizability. Also, because the measure of socioemotional orientation required oncologists to choose between being socioemotional or technical, we could not capture those oncologists who perceived themselves as high on both traits. Finally, because we only audio-recorded visits, we were unable to code nonverbal expressions of patient emotion and oncologist responses. Although nonverbal behaviors are important, oncologists' verbal expressions are least likely to be misunderstood or missed by patients.

Oncologists and patients need to work to create an alliance conducive to patients expressing their emotions. This happens, in part, when oncologists respond empathically when patients express negative emotions. Oncologists, despite their high levels of confidence in addressing emotions, may need more training to recognize emotions and to learn how to respond to patient concerns. Lastly, this relationship is bidirectional. Many empathic opportunities were indirect, and patients may be more satisfied if they can learn how to express their emotions more directly so that oncologists can respond appropriately.


    AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 Author Contributions
 REFERENCES
 
The author(s) indicated no potential conflicts of interest.


    Author Contributions
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 Author Contributions
 REFERENCES
 
Conception and design: Kathryn I. Pollak, Robert M. Arnold, James A. Tulsky

Financial support: Kathryn I. Pollak, James A. Tulsky

Data analysis and interpretation: Kathryn I. Pollak, Robert M. Arnold, Amy S. Jeffreys, Maren K. Olsen, James A. Tulsky

Manuscript writing: Kathryn I. Pollak, Robert M. Arnold, Amy S. Jeffreys, Stewart C. Alexander, Maren K. Olsen, Amy P. Abernethy, Celette Sugg Skinner, Keri L. Rodriguez, James A. Tulsky

Final approval of manuscript: Kathryn I. Pollak, Robert M. Arnold, Stewart C. Alexander, Maren K. Olsen, Amy P. Abernethy, Celette Sugg Skinner, Keri L. Rodriguez, James A. Tulsky


    NOTES
 
Supported by National Cancer Institute Grant No. R01CA100387.

Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 Author Contributions
 REFERENCES
 
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3. Fallowfield LJ, Hall A, Maguire P, et al: Psychological effects of being offered choice of surgery for breast cancer. BMJ 309:448, 1994[Free Full Text]

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6. Ford S, Fallowfield L, Lewis S: Can oncologists detect distress in their out-patients and how satisfied are they with their performance during bad news consultations? Br J Cancer 70:767-770, 1994[Medline]

7. Butow PN, Brown RF, Cogar S, et al: Oncologists' reactions to cancer patients' verbal cues. Psycho-Oncology 11:47-58, 2002[CrossRef][Medline]

8. Goldberg RJ, Mor V: A survey of psychotropic use in terminal cancer patients. Psychosomatics 26:745-748

9. Bukberg J, Penman D, Holland JC: Depression in hospitalized cancer patients. Psychosom Med 46:199-212, 1984[Abstract/Free Full Text]

10. Suchman A, Markakis K, Beckman H, et al: A model of empathic communication in the medical interview. JAMA 277:678-682, 1997[Abstract]

11. Fogarty LA, Curbow BA, Wingard JR, et al: Can 40 seconds of compassion reduce patient anxiety? J Clin Oncol 17:371-379, 1999[Abstract/Free Full Text]

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13. Butow PN, Dunn SM, Tattersall MH, et al: Computer-based interaction analysis of the cancer consultation. Br J Cancer 71:1115-1121, 1995[Medline]

14. Koropchak C, Pollak K, Arnold R, et al: Studying communication in oncologist-patient encounters: The SCOPE Trial. Palliat Med 20:813-819, 2006[Abstract/Free Full Text]

15. Fischer G, Tulsky J, Arnold R: Communicating a poor prognosis, in Portenoy R, Bruera E (eds): Topics in Palliative Care. New York, NY, Oxford University Press, 2000

16. Smith R, Hoppe R: The patient's story: Integrating the patient- and physician-centered approaches to interviewing. Ann Intern Med 115:470-477, 1991[Medline]

17. Tulsky J: Doctor-patient communication issues, in Cassel C, Leipzig R, Cohen H, et al (eds): Geriatric Medicine (ed 4). New York, NY, Springer, 2004

18. Hall JA, Irish JT, Roter DL, et al: Gender in medical encounters: An analysis of physician and patient communication in a primary care setting. Health Psychol 13:384-392, 1994[CrossRef][Medline]

19. Bandura A: Social foundations of thought and action: A social cognitive theory. Englewood Cliffs, NJ, Prentice-Hall, Inc., 1986

20. Buckman R: Breaking bad news: Why is it still so difficult? BMJ Clin Res Ed 288:1597-1599, 1984[Medline]

21. Parle M, Maguire P, Heaven C: The development of a training model to improve health professionals' skills, self-efficacy and outcome expectancies when communicating with cancer patients. Soc Sci Med 44:231-240, 1997[CrossRef][Medline]

22. Block SD, Clark-Chiarelli N, Peters AS, et al: Academia's chilly climate for primary care. JAMA 276:677-682, 1996[Abstract]

23. Baile WF, Lenzi R, Kudelka AP, et al: Improving physician-patient communication in cancer care: Outcome of a workshop for oncologists. J Cancer Educ 12:166-173, 1997[Medline]

24. Ashworth CD, Williamson P, Montano D: A scale to measure physician beliefs about psychosocial aspects of patient care. Soc Sci Med 19:1235-1238, 1984[CrossRef][Medline]

25. Fallowfield L, Jenkins V, Farewell V, et al: Efficacy of a Cancer Res UK communication skills training model for oncologists: A randomised controlled trial. Lancet 359:650-656, 2002[CrossRef][Medline]

26. Levinson W, Gorawara-Bhat R, Lamb J: A study of patient clues and physician responses in primary care and surgical settings. JAMA 284:1021-1027, 2000[Abstract/Free Full Text]

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29. Cabana M, Rand CS, Powe NR, et al: Why don't physicians follow clinical practice guidelines? JAMA 282:1458-1465, 1999[Abstract/Free Full Text]

30. Zinn WM, Block SD, Clark-Chiarelli N: Enthusiasm for primary care: Comparing family medicine and general internal medicine. J Gen Intern Med 13:186-194, 1998[CrossRef][Medline]

Submitted May 1, 2007; accepted September 21, 2007.




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