VOLUME
32
䡠
NUMBER
16
䡠
JUNE
1
2014
JOURNAL OF CLINICAL ONCOLOGY
R E V I E W
A R T I C L E
Overcoming Barriers in Cancer Pain Management Jung Hye Kwon From Kangdong Sacred Heart Hospital, Hallym University, Seoul, Republic of Korea. Published online ahead of print at www.jco.org on May 5, 2014. Author’s disclosures of potential conflicts of interest and author contributions are found at the end of this article. Corresponding author: Jung Hye Kwon, MD, PhD, Division of HematologyOncology, Department of Internal Medicine, Kangdong Sacred Heart Hospital, Hallym University, 150, Sungan-ro, Gangdong-gu, Seoul, 134-701, Republic of Korea; e-mail: [email protected]. © 2014 by American Society of Clinical Oncology 0732-183X/14/3216w-1727w/$20.00
A
B
S
T
R
A
C
T
Pain is a devastating symptom of cancer that affects the quality of life of patients, families, and caregivers. It is a multidimensional symptom that includes physical, psychosocial, emotional, and spiritual components. Despite the development of novel analgesics and updated pain guidelines, cancer pain remains undermanaged, and some patients with moderate to severe pain do not receive adequate pain treatment. Inadequate pain management can be attributed to barriers related to health care professionals, patients, and the health care system. Common professionalrelated barriers include poor pain assessment, lack of knowledge and skill, and the reluctance of physicians to prescribe opioids. Patient-related barriers include cognitive factors, affective factors, and adherence to analgesic regimens. System-related barriers such as limits on access to opioids and the availability of pain and palliative care specialists present additional challenges, particularly in resource-poor regions. Given the multidimensional nature of cancer pain and the multifaceted barriers involved, effective pain control mandates multidisciplinary interventions from interprofessional teams. Educational interventions for patients and health care professionals may improve the success of pain management. J Clin Oncol 32:1727-1733. © 2014 by American Society of Clinical Oncology
DOI: 10.1200/JCO.2013.52.4827
INTRODUCTION
Pain is a distressing symptom of cancer that affects the quality of life of patients, families, and caregivers.1-4 Moderate to severe pain is common throughout the disease trajectory of cancer, and its prevalence increases throughout the course of illness. In fact, such pain has been reported in 59% of patients undergoing anticancer treatment, in 64% of those with advanced/metastatic cancer, and in 33% of those having completed curativetreatment.5,6 Adequatemanagementofcancer pain is the cornerstone of symptom management for patients with cancer. Since the publication of the analgesic ladder by the WHO in 1986, continuing efforts have been made to improve the management of cancer pain through various guidelines and recommendations.7 The National Comprehensive Cancer Network (NCCN) and European Association for Palliative Care research collaborative has also distributed and updated guidelines for cancer pain management.8,9 Initial feasibility and efficacy tests of the WHO analgesic ladder concept have achieved success rates of 71% to 100%.10-12 A 10-year validation study of the WHO analgesic ladder suggested that for the vast majority of patients, cancer pain can be relieved via proper pharmacologic management, with a failure rate of 12%.13 Although cancer pain can often be controlled with proper management, many patients con-
tinue to experience moderate to severe cancer pain, and some do not receive adequate pain medication.5,14-16 In the early 1990s, Cleeland et al14 reported that 42% of patients did not receive adequate pain medication, and 36% experienced impaired function because of pain. The undermanagement of cancer pain has not improved substantially over time.15 A recent European Pain in Cancer survey of adult patients with cancer conducted between 2006 and 2007 reported undermanaged cancer pain.4 In that study, 56% of patients experienced moderate to severe pain (ⱖ 5 of 10 on a numeric rating scale [NRS]) at least several times per month, and 27% rated their pain as severe (ⱖ 7 of 10 on NRS). Moreover, only 24% of patients received strong opioids, and 11% of patients with moderate to severe pain did not receive analgesia. This inadequate pain management led to distress in 67% of patients and the desire for death in 32% of patients. Inadequate cancer pain management is a multidimensional problem. First, pain is a subjective symptom, and physicians have no choice but to rely on patient self-reports. Therefore, the assessment of pain and its response to management can be affected by the patient, the health care professional, and interactions between the two. Second, although opioids represent the cornerstone of management of moderate and severe cancer pain, the prescription of these medications can be influenced by local © 2014 by American Society of Clinical Oncology
Information downloaded from jco.ascopubs.org and provided by at Univ of Texas Libraries on June 1, 2014 from Copyright © 2014 American Society of Clinical Oncology. All rights reserved. 128.83.63.20
1727
Jung Hye Kwon
accessibility as well as attitudes toward and knowledge of opioids among patients and health care professionals. Third, pain is associated with emotional problems and may be linked to other symptoms. For these reasons, a multidimensional approach is needed to evaluate and manage cancer pain. In this article, I will review the main barriers to cancer pain management, specifically health care professional–, patient-, and system-related barriers. I will also discuss potential solutions to overcome these barriers and ultimately improve cancer pain management.
LITERATURE REVIEW
The literature search was performed independently by a librarian of Kangdong Sacred Hospital (S.H. Kim) and the author in Medline during the period of 1986 to 2013. The medical subject headings and key words used for the search were cancer, tumor, malignancy, pain, neuropathic pain, patient, physician, oncology, barriers, pain management, pain control, opioid, and analgesia. The last search was carried out in June 2013. Only articles in English were considered, and original reports, review articles, guidelines, meta-analyses, systematic reviews, editorials, commentaries, and letters were included. Articles in languages other than English and case reports were excluded.
BARRIERS TO CANCER PAIN MANAGEMENT FROM THE PERSPECTIVE OF PHYSICIANS
The undermedication of cancer pain is a common unsolved problem in the management of patients with cancer, and physicians seem to be aware of this problem. Most physicians who participated in survey-based studies reported that patients with cancer were undermanaged, and this perception remained mostly unchanged over time but varied greatly by geographic region. In 1990, 86% of US physicians who participated in a survey conducted by the Eastern Cooperative Oncology Group (ECOG) reported that many patients with cancer were undermanaged,17 and 7 years later, 83% of the members of the radiation oncology therapy group still believed that patients were undertreated for pain.18 In Israel in the mid 1990s, 58% of physicians believed that cancer pain could be managed in more than 75% of patients, but only 17% reported that they were capable of achieving this target in their own practice.19 More recently, approximately half of Finnish physicians believed that cancer pain was well managed in their practice (47% of oncologists and 61% of other physicians),20 and more than half of a group of French physicians surveyed (including 51% of oncologists and 60% of primary care physicians) were satisfied with cancer pain management in their country.21 Physician-related reasons for the undermedication of cancer pain have been studied. The majority of these studies either asked physicians to select from a list of barriers or provided open-ended questions. Although variation exists among the studies, frequently reported barriers included poor pain assessment, a lack of knowledge among staff, a reluctance of physicians to prescribe opioids, legal or administrative constraints, a reluctance of patients to take opioids, and a reluctance of patients to report their pain (Table 1). 1728
© 2014 by American Society of Clinical Oncology
Table 1. Barriers to Cancer Pain Management From the Perspective of Professionals Barrier Related to professional Poor pain assessment Lack of knowledge Reluctance to prescribe opioids Fear of adverse effects Risk of tolerance Fear of drug addiction Fear of legal/administrative constraints Excessive regulation of opioids at pharmacy Perception that nonopioid analgesics have same efficacy as opioid analgesics Perception of negative public image of morphine Nursing staff reluctance to administer opioids Discrepancy between self-evaluation and knowledge Lack of specialists Related to patient Patient reluctance to report pain Patient reluctance to take opioids Patient inability to pay for analgesics Related to health care system Lack of neurodestructive procedures Lack of psychosocial support services Lack of equipment or skills Lack of access to wide range of analgesics Lack of access to professional methods Difficulty in accessing services to enable nonpharmacologic pain management Impact of distance on ability to access pain-related services Lack of coordination across multiple providers Difficulty in accessing interventional pain services Lack of support from specialist in pain and palliative care Inadequate guidance of pain specialist Lack of access to wide range of opioids Lack of staff time to attend to pain needs of patient
Poor Pain Assessment Inadequate assessment of pain is the barrier to cancer pain management that has been most frequently mentioned by physicians.17-20,22 The expression of pain by patients is the only source of information for pain evaluation. Use of standardized pain assessment tools allows clinicians to assess this subjective symptom in a reliable and valid manner. The visual analog scale (VAS) and NRS are simple and easy to use; however, only 7% to 43% of physicians use one of these scales in their practice, and multidimensional questionnaires are rarely used.20,23-25 Alarmingly, 30% to 51% of physicians thought that patients exaggerated their pain to attract attention.26 Moreover, only a small number of physicians reported applying pain management guidelines in their practice.19,23 Physicians’ Reluctance to Administer Opioids The literature shows that 23% to 31% of physicians tended to delay strong opioids until patients reached the terminal phase of their disease or until their pain became intractable. This reluctance to use opioids was higher among primary care physicians than among oncologists,17,18,21,27,28 and oncologists rated their peers as being more conservative in terms of the prescription of opioids.22 In cases of severe JOURNAL OF CLINICAL ONCOLOGY
Information downloaded from jco.ascopubs.org and provided by at Univ of Texas Libraries on June 1, 2014 from Copyright © 2014 American Society of Clinical Oncology. All rights reserved. 128.83.63.20
Overcoming Barriers in Cancer Pain Management
cancer pain, only approximately half of physicians chose to treat using strong opioids.17,18,26 A number of physician characteristics were related to the early aggressive management of cancer pain: recent training, use of VAS or NRS for pain evaluation, less fear of addiction, self-evaluation as a medical oncologist (v non–medical oncologist), viewing pain relief as a goal of treatment, seeing themselves as liberal in pain management, and attributing patient requests to elevate dosage to increased pain rather than addiction.17,24 Lack of Knowledge Investigations into physician knowledge of cancer pain management have been conducted in various ways, from asking questions on the concepts of guidelines to asking detailed questions based on clinical conditions. Oncologists showed a greater basic knowledge of cancer pain management than did other specialists (eg, general practitioners, internal medicine specialists, and geriatric specialists); however, more than half of oncologists failed to correctly answer questions based on case scenarios.20 With respect to basic knowledge, 13% to 68% of physicians were familiar with the WHO guidelines or other cancer pain management guidelines, but the level of understanding varied among physicians.20,29,30 The following topics have been identified as areas of knowledge deficiency among physicians: regular medication for chronic cancer pain (42%), the pathophysiology of cancer pain (especially neuropathic pain), equianalgesic dose and dose titration, breakthrough pain, adjuvant medications, addiction, and tolerance.19,21,25,28,29,31,32 Discrepancy Between Perception and Reality Physicians reported that cancer pain was poorly managed in clinical practice, and this finding correlates well with reports on the prevalence of undermanaged cancer pain.5,15 Paradoxically, physicians often self-reported that they had a good working knowledge of cancer pain and its management. For example, 78% to 93% of oncologists reported having a strong knowledge of cancer pain, which is higher than the percentage reported by other specialists.18,21,22,31 When tested, oncologists were found to have a good general knowledge (eg, familiarity with WHO guidelines), but they scored poorly when asked about specific clinical situations.20,22 This discrepancy between self-assessment and actual practice indicates that physicians may not fully realize their knowledge deficiencies, which could represent a potential barrier to cancer pain management. Other Barriers to Cancer Pain Management A fear of addiction is one barrier that explains why physicians are reluctant to prescribe opioids. It has been shown that 25% to 40% of physicians worry about addiction, and this rate was higher for patients with a family history of addiction.21,27 The risk of tolerance (requiring ever-higher doses of opioids), requirement for opioid prescriptions to be written on special prescription forms, and negative perception of opioids were some of the key barriers for physicians.19,21,29,33 In terms of its role as a barrier to cancer pain management, the fear of regulation is experienced quite differently in China compared with other countries. Approximately 75% of Chinese physicians stated that excessive state regulation of opioid prescription was one of the major barriers to cancer pain management, whereas 8% to 27% of physicians in Western countries described this factor as a barrier to cancer pain management.17-21,23,26,28,29,33 Regulatory constraints on opioid prescription differ widely among countries, with physicians in www.jco.org
developed countries having access to a wide range of opioids and those in developing countries having limited treatment options. Surveys of US medical oncologist in 2009 and of Australian oncologists in 2011 and 2012 revealed that a majority of physicians did not refer patients to pain or palliative care specialists because of difficulties in accessing or scheduling appointments with these services.22,23 Interventions to Address Professional Barriers to Cancer Pain Management Intervention studies to improve cancer pain management on the professional side included professional education, pain assessment, and consultation with a specialist. Professional intervention for nurses has been reported to improve the knowledge and attitude of the nurses after education; however, no study has shown that this improvement in knowledge results in an improvement in pain management.34-36 Schmerz-Therapie in der Onkologischen Paediatrie (STOP), a nationwide quality improvement program on pediatric oncology pain control from 1997 to 2001 in Germany, showed promising results for improving knowledge and practice.37 This study compared pain management in pediatric oncology practices between active quality management (QM) departments and nonactive QM departments. Both study arms received training and a manual based on contemporary pain practices, and the active QM departments also had in-depth training and periodic feedback. Eight departments (36 participants) were enrolled in the active QM arm, and 64 departments (193 participants) were enrolled in the nonactive QM arm. The participants included head physicians, ward physicians, head nurses, and psychologists/social workers. Active QM departments showed improvements in the knowledge of pain control and neuropathic pain among health care professionals, including the use of less painful modes of administration and a reduction in the usage of mixed opioid agonists-antagonists in their practice. Patients between ages 12 and 17 years and parents of patients younger than age 12 years in the active QM arm indicated decreased pain intensity and decreased incidence of severe pain. According to the participant self-assessments, STOP improved practical pain management in the active QM departments, whereas the change was negligible in the nonactive QM departments. ECOG also conducted a study to compare the effectiveness of a standardized analgesic protocol for cancer pain management versus leaving pain management to the discretion of the treating physician. In a group of patients with lung or prostate cancer, the proportion of pain reduction of the worst pain was higher in the analgesic protocol group than in the physician discretion group at 2-week follow-up (48% v 15%; P ⬍ .001), and this difference was maintained 4 weeks later (52% v 19%; P ⫽ .045). The worst pain was reduced by 27% in the analgesic protocol group. Although the study was closed early because of poor accrual, the analgesic protocol group exhibited better pain control.38 BARRIERS TO CANCER PAIN MANAGEMENT FROM THE PERSPECTIVE OF PATIENTS
Cognitive barriers, affective barriers, and nonadherence to pain medication represent some common patient-related factors that can decrease the effectiveness of cancer pain management (Table 2). © 2014 by American Society of Clinical Oncology
Information downloaded from jco.ascopubs.org and provided by at Univ of Texas Libraries on June 1, 2014 from Copyright © 2014 American Society of Clinical Oncology. All rights reserved. 128.83.63.20
1729
Jung Hye Kwon
Table 2. Barriers to Pain Management From the Perspective of Patients Barrier Cognitive Concern regarding disease progression Concern regarding addiction Concern over development of tolerance Adverse effects Idea of being a good patient Fatalistic belief regarding cancer pain Concern about distracting physician from cancer care Fear of injections Harmful for immune system Affective Adherence to medication
Cognitive Barriers to Cancer Pain Management Because pain is a subjective symptom, a patient’s attitude toward and knowledge of cancer pain and its management may influence pain assessment and its related outcomes. A patient who has concerns and misconceptions about pain medications be reluctant to report pain and take opioids. Other potential barriers from the patient perspective may include miscommunication with physicians (under-reporting of symptoms to avoid distracting physician from providing cancer treatments), misconceptions regarding pain medicine (fear of adverse effects, addiction, tolerance, and lowered immunity caused by pain medicine), and fatalistic beliefs (inevitably, uncontrollability, and idea that increasing pain indicates disease progression). These patientrelated barriers to cancer pain management have been studied using a 27-item self-reported questionnaire developed specifically for the purpose and then subsequently modified to generate the Barriers Questionnaire II.39,40 Patient-related barriers to cancer pain management can be associated with poor quality of life, poor pain control according to a pain management index (calculated by subtracting pain intensity score [none, 0; mild, 1; moderate, 2; severe, 3] from analgesic usage score [0, no analgesics; 1, nonopioid analgesics; 2, weak opioids; 3, strong opioids], with negative score indicating inadequate management), and negative mood (ie, depression).39-41 Patient-related barriers to cancer pain management vary among cultures. According to a meta-analysis by Chen et al,42 Asian patients perceived greater barriers to managing cancer pain than did Western patients, particularly with respect to concerns about disease progression, tolerance, and fatalism. Affective Barriers to Cancer Pain Management Psychological distress has been shown to be significantly associated with the perception of pain.43 Higher pain intensity was associated with a higher level of psychological distress, including depression, anxiety, hostility, mood disturbances, and anger.44 Our recent study on patient-reported barriers to cancer pain management in oncology clinics revealed that higher scores on the Beck Depression Inventory were associated with higher scores on the Barriers Questionnaire II in a multivariable regression analysis.41 A study by Wang et al45 suggested that a greater improvement of depression was one of the predictors of cancer-related pain improvement over time. Testing positive with regard to depression 1730
© 2014 by American Society of Clinical Oncology
according to the Patient Health Questionnaire–2 was also reported to be associated with poorer medication adherence in patients with advanced lung cancer.46 Given the importance of psychological well-being in pain management, routine screening for depression and anxiety should be part of initial pain assessment. Adherence to Pain Medications Adherence to pain medication was also related to the outcome of pain management. Adherence to regular opioids was reported to be 63% to 91%, and adherence to as-needed medications was reported to be 22% to 27%.47-49 In a study of Taiwanese outpatients with cancer, negative beliefs regarding opioid analgesics were associated with low opioid adherence (r ⫽ ⫺0.3; P ⬍ .01). Furthermore, the opioid-taking self-efficacy of patients (self-efficacy defined as belief or confidence in one’s capability to carry out a certain behavior to produce a desired outcome) was positively correlated with opioid adherence (r ⫽ 0.22; P ⬍ .05) and pain relief (r ⫽ 0.35; P ⬍ .01). The opioid-taking self-efficacy of patients was the only significant predictor of pain relief in a hierarchic multiple regression analysis that included sex, education, and beliefs about analgesics as independent factors (explaining 11% of variance; P ⫽ .001).47 Another study of patients with cancer revealed that better adherence to provider-recommended treatments was associated with less-severe pain.48 Regular follow-up appointments to assess adherence to analgesic medication are important to achieve good pain management. The cost of opioids also varies by country, and some patients have difficulty paying for their prescriptions.50 Interventions to Address Patient-Related Barriers to Cancer Pain Management Patient-based educational interventions have been postulated to facilitate better cancer pain management through changes in knowledge, attitudes, and beliefs. A meta-analysis of 21 randomized trials by Bennett et al51 was conducted to determine the effects of various interventions on cancer pain management. Patient education had a positive effect on patient knowledge of cancer pain management (P ⫽ .008) and resulted in a statistically significant reduction in average pain intensity (0 to 10 NRS from the Brief Pain Inventory), with a 1.1-point reduction in the worst pain experienced by patients. However, the intervention showed no significant effects on mood or quality of life. Most of the interventions consisted of face-to-face coaching sessions (15 to 60 minutes) with an informational booklet. No consistent effects were detected regarding medication adherence or self-efficacy. This study suggested that intervention has modest effects on pain intensity, attitude, and knowledge relative to usual care based on the results of the meta-analysis. A recent randomized controlled trial52 of a tailored education and coaching (TEC) intervention was conducted in patients with cancer with moderate pain and functional impairment in an attempt to enhance the management of cancer-related pain through patient education and coaching. Communication self-efficacy was improved in the TEC group (P ⬍ .001). However, pain misconceptions decreased in both groups, and no statistically significant difference was detected; pain misconceptions were significantly reduced to a similar degree in both groups (P ⬍ .001). Improvement in pain-related impairment (⫺0.25 points on 5-point scale; 95% CI, ⫺0.43 to ⫺0.06; JOURNAL OF CLINICAL ONCOLOGY
Information downloaded from jco.ascopubs.org and provided by at Univ of Texas Libraries on June 1, 2014 from Copyright © 2014 American Society of Clinical Oncology. All rights reserved. 128.83.63.20
Overcoming Barriers in Cancer Pain Management
P ⫽ .01) in the TEC group was only observed at the 2-week follow-up, but this improvement was not sustained at 6 or 12 weeks. TEC had no significant effect on the reduction of pain severity or improvement in functional status or well-being. There is good evidence to support the role of patient education in cancer pain management. However, there is wide variation among existing interventions, making it difficult to provide a specific recommendation in the absence of data that can be used to make direct comparisons. Future studies should examine the optimal components of patient education and identify the most effective program. BARRIERS TO CANCER PAIN MANAGEMENT FROM SYSTEMIC PERSPECTIVES
Barriers Related to Opioids The range of available drugs and accessibility of opioids for cancer pain vary according to country. Physicians in developed countries may experience fewer constraints from legal or regulatory bodies, whereas those who practice in developing countries often have to deal with more restrictions on opioid prescriptions. Less than 50% of physicians in France, Canada, and the United States felt that prescribing opioids was inconvenient or that their opioid prescriptions for cancer pain were influenced by regulation, whereas more than 70% of Chinese physicians perceived a limitation on their ability to prescribe opioids because of strong regulation.17,29-31 However, even US physicians have misconceptions about regulatory monitoring; for example, almost 50% of physicians surveyed were concerned that too many narcotic prescriptions would lead to utilization reviews by a regulatory agency.27 Barriers Related to the Health Care System Multidimensional pain control requires collaboration with other specialists, especially palliative care physicians. Surveys of physicians revealed barriers to the access of pain and palliative care specialists.17,18,23 Physicians reported difficulty accessing other health care professionals, including specialists in neurodestructive procedures (5% to 31%), interventional pain services (88%), psychosocial support (11% to 54%), and nonpharmacologic pain management (88%). Some physicians perceived difficulty accessing specialists because of the physical distance between their practice and the specialist services.17,18,23,28,33 Barriers Related to Education A majority of physicians surveyed reported that education on cancer pain management during medical school and residency training was poor and that more extensive training was necessary in Denmark,53 Finland,20 France,21 Israel,19 South Korea,26 Sweden,25 Taiwan,28 China,29 and the United States.17 Of the participants, 10% to 19% (n ⫽ 879) were satisfied with their pain-related education during medical school, and 52% to 67% rated it as poor.17,19,53 More than half of physicians reported that they had not received training in cancer pain management.21 The evaluation of pain education was better for physicians who had received education and training recently than for older physicians with regard to both medical school and residency training (P ⫽ .01).22 Only 20% to 25% hematology-oncology fellows completed a mandatory palliative care rotation during their www.jco.org
fellowship,54 and education on pain management remained limited even for these trainees.55
STRATEGIES TO OVERCOME BARRIERS TO CANCER PAIN MANAGEMENT
Cancer pain is a multidimensional symptom with both physical and nonphysical components. Adequate pain control requires a multidimensional approach toward assessment and management. Barriers to cancer pain management are also multidimensional in nature and include patient-, physician-, and system-related factors. Successful management of cancer pain therefore mandates multidisciplinary interventions by interprofessional teams.56-58 The following list of recommendations may help address some common barriers to cancer pain management.59-61 Assessment of pain and outcome ● Using validated pain tools for screening and monitoring (eg, NRS and VAS) ● Providing multidimensional evaluation, including physical, functional, psychosocial, and spiritual aspects (eg, Edmonton Symptom Assessment System or Edmonton Classification System for Cancer Pain) ● Evaluating comorbidities ● Ongoing assessment of pain with regular follow-up appointments Management of cancer pain ● Abiding by current updated guidelines (eg, WHO guidelines, NCCN guidelines, and American Pain Society guidelines) ● Choosing appropriate analgesics with adequate dosages, routes, and schedules ● Choosing adequate adjuvant analgesics according to pain pathophysiology ● Monitoring the outcome after starting analgesics ● Anticipating and treating analgesic adverse effects ● Collaborating with other specialties, especially palliative care physicians, for a multidisciplinary approach Education of patients and family members ● Informing patients that most cancer pain can be alleviated, while also setting realistic expectations and pain goals ● Providing psychosocial support ● Providing patient and family caregiver education on the appropriate use of pain medications ● Providing patients with pain and medication diaries Education of physicians and health care professionals ● Didactic lectures and rotations on pain management and palliative care for students and trainees ● Continuing medical education on pain topics for practicing clinicians ● Interdisciplinary pain management rounds to discuss patient cases ● Increased training of pain and palliative care specialists Overcoming system-based issues ● Advocacy for increased availability to opioids in countries with limited access ● Increase availability of pain and palliative care services © 2014 by American Society of Clinical Oncology
Information downloaded from jco.ascopubs.org and provided by at Univ of Texas Libraries on June 1, 2014 from Copyright © 2014 American Society of Clinical Oncology. All rights reserved. 128.83.63.20
1731
Jung Hye Kwon
DISCUSSION
Cancer pain is a multidimensional symptom that is frequently undermanaged. Barriers to cancer management have many facets, including patients, health care providers, and the system. This multifaceted nature of barriers in cancer pain management might be the reason for the failure of most one-sided barrier-approach studies. A multidirectional interdisciplinary approach might be the best way to improve cancer pain management by overcoming REFERENCES 1. Yamagishi A, Morita T, Miyashita M, et al: Pain intensity, quality of life, quality of palliative care, and satisfaction in outpatients with metastatic or recurrent cancer: A Japanese, nationwide, regionbased, multicenter survey. J Pain Symptom Manage 43:503-514, 2012 2. Koyyalagunta D, Bruera E, Solanki DR, et al: A systematic review of randomized trials on the effectiveness of opioids for cancer pain. Pain Physician 15:ES39-ES58, 2012 (suppl 3) 3. Valdimarsdo´ttir U, Helgason AR, Fu¨rst CJ, et al: The unrecognised cost of cancer patients’ unrelieved symptoms: A nationwide follow-up of their surviving partners. Br J Cancer 86:1540-1545, 2002 4. Breivik H, Cherny N, Collett B, et al: Cancerrelated pain: A pan-European survey of prevalence, treatment, and patient attitudes. Ann Oncol 20: 1420-1433, 2009 5. van den Beuken-van Everdingen MH, de Rijke JM, Kessels AG, et al: Prevalence of pain in patients with cancer: A systematic review of the past 40 years. Ann Oncol 18:1437-1449, 2007 6. van den Beuken-van Everdingen MH, de Rijke JM, Kessels AG, et al: High prevalence of pain in patients with cancer in a large population-based study in the Netherlands. Pain 132:312-320, 2007 7. World Health Organization: Cancer Pain Relief. Geneva, Switzerland, World Health Organization, 1986 8. National Comprehensive Cancer Network: NCCN clinical practice guidelines in oncology. http:// www.nccn.org/professionals/physician_gls/ f_guidelines.asp#supportive 9. Caraceni A, Hanks G, Kaasa S, et al: Use of opioid analgesics in the treatment of cancer pain: Evidence-based recommendations from the EAPC. Lancet Oncol 13:e58-e68, 2012 10. Takeda F: Results of field-testing in Japan of the WHO draft interim guidelines on relief of cancer pain. http://apps.who.int/iris/handle/10665/60895? mode⫽full&submit_simple⫽Show⫹full⫹item⫹record 11. Ventafridda V, Tamburini M, Caraceni A, et al: A validation study of the WHO method for cancer pain relief. Cancer 59:850-856, 1987 12. Walker VA, Hoskin PJ, Hanks GW, et al: Evaluation of WHO analgesic guidelines for cancer pain in a hospital-based palliative care unit. J Pain Symptom Manage 3:145-149, 1988 13. Zech DF, Grond S, Lynch J, et al: Validation of World Health Organization guidelines for cancer pain relief: A 10-year prospective study. Pain 63:65-76, 1995 14. Cleeland CS, Gonin R, Hatfield AK, et al: Pain and its treatment in outpatients with metastatic cancer. N Engl J Med 330:592-596, 1994 15. Deandrea S, Montanari M, Moja L, et al: Prevalence of undertreatment in cancer pain: A 1732
© 2014 by American Society of Clinical Oncology
barriers. Moreover, pain management education should be provided to physicians throughout medical school, residency, fellowship, and practice.
AUTHOR’S DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST The author(s) indicated no potential conflicts of interest.
review of published literature. Ann Oncol 19:19851991, 2008 16. Hong SH, Roh SY, Kim SY, et al: Change in cancer pain management in Korea between 2001 and 2006: Results of two nationwide surveys. J Pain Symptom Manage [epub ahead of print on September 24, 2010] 17. von Roenn JH, Cleeland CS, Gonin R, et al: Physician attitudes and practice in cancer pain management: A survey from the Eastern Cooperative Oncology Group. Ann Intern Med 119:121-126, 1993 18. Cleeland CS, Janjan NA, Scott CB, et al: Cancer pain management by radiotherapists: A survey of radiation therapy oncology group physicians. Int J Radiat Oncol Biol Phys 47:203-208, 2000 19. Sapir R, Catane R, Strauss-Liviatan N, et al: Cancer pain: Knowledge and attitudes of physicians in Israel. J Pain Symptom Manage 17:266-276, 1999 20. Silvoniemi M, Vasankari T, Vahlberg T, et al: Physicians’ self-assessment of cancer pain treatment skills: More training required. Support Care Cancer 20:2747-2275, 2012 21. Larue F, Colleau SM, Fontaine A, et al: Oncologists and primary care physicians’ attitudes toward pain control and morphine prescribing in France. Cancer 76:2375-2382, 1995 22. Breuer B, Fleishman SB, Cruciani RA, et al: Medical oncologists’ attitudes and practice in cancer pain management: A national survey. J Clin Oncol 29:4769-4775, 2011 23. Luckett T, Davidson PM, Boyle F, et al: Australian survey of current practice and guideline use in adult cancer pain assessment and management: Perspectives of oncologists. Asia Pac J Clin Oncol [epub ahead of print on December 17, 2012] 24. Yun YH, Park SM, Lee K, et al: Predictors of prescription of morphine for severe cancer pain by physicians in Korea. Ann Oncol 16:966-971, 2005 25. Rawal N, Hylander J, Arne´r S: Management of terminal cancer pain in Sweden: A nationwide survey. Pain 54:169-179, 1993 26. Kim MH, Park H, Park EC, et al: Attitude and knowledge of physicians about cancer pain management: Young doctors of South Korea in their early career. Jpn J Clin Oncol 41:783-791, 2011 27. Weinstein SM, Laux LF, Thornby JI, et al: Physicians’ attitudes toward pain and the use of opioid analgesics: Results of a survey from the Texas Cancer Pain Initiative. South Med J 93:479487, 2000 28. Ger LP, Ho ST, Wang JJ: Physicians’ knowledge and attitudes toward the use of analgesics for cancer pain management: A survey of two medical centers in Taiwan. J Pain Symptom Manage 20:335344, 2000 29. Yanjun S, Changli W, Ling W, et al: A survey on physician knowledge and attitudes towards clinical use of morphine for cancer pain treatment in China. Support Care Cancer 18:1455-1460, 2010
30. Wolfert MZ, Gilson AM, Dahl JL, et al: Opioid analgesics for pain control: Wisconsin physicians’ knowledge, beliefs, attitudes, and prescribing practices. Pain Med 11:425-434, 2010 31. Gallagher R, Hawley P, Yeomans W: A survey of cancer pain management knowledge and attitudes of British Columbian physicians. Pain Res Manag 9:188-194, 2004 32. Larue F, Colleau SM, Brasseur L, et al: Multicentre study of cancer pain and its treatment in France. BMJ 310:1034-1037, 1995 33. Yu S, Wan XS, Cheng Y, et al: Special aspects of cancer pain management in a Chinese general hospital. Eur J Pain 5:15-20, 2001 (suppl A) 34. Huth MM, Gregg TL, Lin L: Education changes Mexican nurses’ knowledge and attitudes regarding pediatric pain. Pain Manag Nurs 11:201208, 2010 35. Ger LP, Chang CY, Ho ST, et al: Effects of a continuing education program on nurses’ practices of cancer pain assessment and their acceptance of patients’ pain reports. J Pain Symptom Manage 27:61-71, 2004 36. Vallerand AH, Riley-Doucet C, Hasenau SM, et al: Improving cancer pain management by homecare nurses. Oncol Nurs Forum 31:809-816, 2004 37. Zernikow B, Hasan C, Hechler T, et al: Stop the pain! A nation-wide quality improvement programme in paediatric oncology pain control. Eur J Pain 12:819-833, 2008 38. Cleeland CS, Portenoy RK, Rue M, et al: Does an oral analgesic protocol improve pain control for patients with cancer? An intergroup study coordinated by the Eastern Cooperative Oncology Group. Ann Oncol 16:972-980, 2005 39. Ward SE, Goldberg N, Miller-McCauley V, et al: Patient-related barriers to management of cancer pain. Pain 52:319-324, 1993 40. Gunnarsdottir S, Donovan HS, Serlin RC, et al: Patient-related barriers to pain management: The Barriers Questionnaire II (BQ-II). Pain 99:385-396, 2002 41. Kwon JH, Oh SY, Chisholm G, et al: Predictors of high score patient-reported barriers to controlling cancer pain: A preliminary report. Support Care Cancer 21:1175-1183, 2013 42. Chen CH, Tang ST, Chen CH: Meta-analysis of cultural differences in Western and Asian patientperceived barriers to managing cancer pain. Palliat Med 26:206-221, 2012 43. Delgado-Guay M, Parsons HA, Li Z, et al: Symptom distress in advanced cancer patients with anxiety and depression in the palliative care setting. Support Care Cancer 17:573-579, 2009 44. Zaza C, Baine N: Cancer pain and psychosocial factors: A critical review of the literature. J Pain Symptom Manage 24:526-542, 2002 45. Wang HL, Kroenke K, Wu J, et al: Predictors of cancer-related pain improvement over time. Psychosom Med 74:642-647, 2012 JOURNAL OF CLINICAL ONCOLOGY
Information downloaded from jco.ascopubs.org and provided by at Univ of Texas Libraries on June 1, 2014 from Copyright © 2014 American Society of Clinical Oncology. All rights reserved. 128.83.63.20
Overcoming Barriers in Cancer Pain Management
46. Yoong J, Traeger LN, Gallagher ER, et al: A pilot study to investigate adherence to long-acting opioids among patients with advanced lung cancer. J Palliat Med 16:391-396, 2013 47. Liang SY, Yates P, Edwards H, et al: Factors influencing opioid-taking self-efficacy and analgesic adherence in Taiwanese outpatients with cancer. Psychooncology 17:1100-1107, 2008 48. Jerant A, Franks P, Tancredi DJ, et al: Tendency to adhere to provider-recommended treatments and subsequent pain severity among individuals with cancer. Patient Prefer Adherence 5:23-31, 2011 49. Valeberg BT, Miaskowski C, Hanestad BR, et al: Prevalence rates for and predictors of selfreported adherence of oncology outpatients with analgesic medications. Clin J Pain 24:627-636, 2008 50. Dalal S, Bruera E: Access to opioid analgesics and pain relief for patients with cancer. Nat Rev Clin Oncol 10:108-116, 2013
51. Bennett MI, Bagnall AM, Jose´ Closs S: How effective are patient-based educational interventions in the management of cancer pain? Systematic review and meta-analysis. Pain 143:192-199, 2009 52. Kravitz RL, Tancredi DJ, Grennan T, et al: Cancer Health Empowerment for Living without Pain (Ca-HELP): Effects of a tailored education and coaching intervention on pain and impairment. Pain 152:1572-1582, 2011 53. Sjøgren P, Banning AM, Jensen NH, et al: Management of cancer pain in Denmark: A nationwide questionnaire survey. Pain 64:519-525, 1996 54. Hui D, Elsayem A, De la Cruz M, et al: Availability and integration of palliative care at US cancer centers. JAMA 303:1054-1061, 2010 55. Buss MK, Lessen DS, Sullivan AM, et al: Hematology/oncology fellows’ training in palliative
care: Results of a national survey. Cancer 117:43044311, 2011 56. McNeill JA, Sherwood GD, Starck PL: The hidden error of mismanaged pain: A systems approach. J Pain Symptom Manage 28:47-58, 2004 57. Fairchild A: Under-treatment of cancer pain. Curr Opin Support Palliat Care 4:11-15, 2010 59. Zuccaro SM, Vellucci R, Sarzi-Puttini P, et al: Barriers to pain management: Focus on opioid therapy. Clin Drug Investig 32:11-19, 2012 (suppl 1) 60. Green E, Zwaal C, Beals C, et al: Cancerrelated pain management: A report of evidencebased recommendations to guide practice. Clin J Pain 26:449-462, 2010 61. Sun VC, Borneman T, Ferrell B, et al: Overcoming barriers to cancer pain management: An institutional change model. J Pain Symptom Manage 34:359-369, 2007
■ ■ ■
Conquer Cancer Foundation of the American Society of Clinical Oncology The Conquer Cancer Foundation (CCF) was created by foremost cancer physicians of the American Society of Clinical Oncology to seek dramatic advances in the prevention, treatment, and cures of all types of cancer. Working toward the vision of a world free from the fear of cancer, CCF strives to conquer this disease by funding breakthrough cancer research and sharing cutting-edge knowledge with patients and physicians worldwide, by improving quality of and access to care, and by enhancing quality of life for all who are touched by cancer. For more information, visit www.conquercancerfoundation.org.
www.jco.org
© 2014 by American Society of Clinical Oncology
Information downloaded from jco.ascopubs.org and provided by at Univ of Texas Libraries on June 1, 2014 from Copyright © 2014 American Society of Clinical Oncology. All rights reserved. 128.83.63.20
1733
32
䡠
NUMBER
16
䡠
JUNE
1
2014
JOURNAL OF CLINICAL ONCOLOGY
R E V I E W
A R T I C L E
Overcoming Barriers in Cancer Pain Management Jung Hye Kwon From Kangdong Sacred Heart Hospital, Hallym University, Seoul, Republic of Korea. Published online ahead of print at www.jco.org on May 5, 2014. Author’s disclosures of potential conflicts of interest and author contributions are found at the end of this article. Corresponding author: Jung Hye Kwon, MD, PhD, Division of HematologyOncology, Department of Internal Medicine, Kangdong Sacred Heart Hospital, Hallym University, 150, Sungan-ro, Gangdong-gu, Seoul, 134-701, Republic of Korea; e-mail: [email protected]. © 2014 by American Society of Clinical Oncology 0732-183X/14/3216w-1727w/$20.00
A
B
S
T
R
A
C
T
Pain is a devastating symptom of cancer that affects the quality of life of patients, families, and caregivers. It is a multidimensional symptom that includes physical, psychosocial, emotional, and spiritual components. Despite the development of novel analgesics and updated pain guidelines, cancer pain remains undermanaged, and some patients with moderate to severe pain do not receive adequate pain treatment. Inadequate pain management can be attributed to barriers related to health care professionals, patients, and the health care system. Common professionalrelated barriers include poor pain assessment, lack of knowledge and skill, and the reluctance of physicians to prescribe opioids. Patient-related barriers include cognitive factors, affective factors, and adherence to analgesic regimens. System-related barriers such as limits on access to opioids and the availability of pain and palliative care specialists present additional challenges, particularly in resource-poor regions. Given the multidimensional nature of cancer pain and the multifaceted barriers involved, effective pain control mandates multidisciplinary interventions from interprofessional teams. Educational interventions for patients and health care professionals may improve the success of pain management. J Clin Oncol 32:1727-1733. © 2014 by American Society of Clinical Oncology
DOI: 10.1200/JCO.2013.52.4827
INTRODUCTION
Pain is a distressing symptom of cancer that affects the quality of life of patients, families, and caregivers.1-4 Moderate to severe pain is common throughout the disease trajectory of cancer, and its prevalence increases throughout the course of illness. In fact, such pain has been reported in 59% of patients undergoing anticancer treatment, in 64% of those with advanced/metastatic cancer, and in 33% of those having completed curativetreatment.5,6 Adequatemanagementofcancer pain is the cornerstone of symptom management for patients with cancer. Since the publication of the analgesic ladder by the WHO in 1986, continuing efforts have been made to improve the management of cancer pain through various guidelines and recommendations.7 The National Comprehensive Cancer Network (NCCN) and European Association for Palliative Care research collaborative has also distributed and updated guidelines for cancer pain management.8,9 Initial feasibility and efficacy tests of the WHO analgesic ladder concept have achieved success rates of 71% to 100%.10-12 A 10-year validation study of the WHO analgesic ladder suggested that for the vast majority of patients, cancer pain can be relieved via proper pharmacologic management, with a failure rate of 12%.13 Although cancer pain can often be controlled with proper management, many patients con-
tinue to experience moderate to severe cancer pain, and some do not receive adequate pain medication.5,14-16 In the early 1990s, Cleeland et al14 reported that 42% of patients did not receive adequate pain medication, and 36% experienced impaired function because of pain. The undermanagement of cancer pain has not improved substantially over time.15 A recent European Pain in Cancer survey of adult patients with cancer conducted between 2006 and 2007 reported undermanaged cancer pain.4 In that study, 56% of patients experienced moderate to severe pain (ⱖ 5 of 10 on a numeric rating scale [NRS]) at least several times per month, and 27% rated their pain as severe (ⱖ 7 of 10 on NRS). Moreover, only 24% of patients received strong opioids, and 11% of patients with moderate to severe pain did not receive analgesia. This inadequate pain management led to distress in 67% of patients and the desire for death in 32% of patients. Inadequate cancer pain management is a multidimensional problem. First, pain is a subjective symptom, and physicians have no choice but to rely on patient self-reports. Therefore, the assessment of pain and its response to management can be affected by the patient, the health care professional, and interactions between the two. Second, although opioids represent the cornerstone of management of moderate and severe cancer pain, the prescription of these medications can be influenced by local © 2014 by American Society of Clinical Oncology
Information downloaded from jco.ascopubs.org and provided by at Univ of Texas Libraries on June 1, 2014 from Copyright © 2014 American Society of Clinical Oncology. All rights reserved. 128.83.63.20
1727
Jung Hye Kwon
accessibility as well as attitudes toward and knowledge of opioids among patients and health care professionals. Third, pain is associated with emotional problems and may be linked to other symptoms. For these reasons, a multidimensional approach is needed to evaluate and manage cancer pain. In this article, I will review the main barriers to cancer pain management, specifically health care professional–, patient-, and system-related barriers. I will also discuss potential solutions to overcome these barriers and ultimately improve cancer pain management.
LITERATURE REVIEW
The literature search was performed independently by a librarian of Kangdong Sacred Hospital (S.H. Kim) and the author in Medline during the period of 1986 to 2013. The medical subject headings and key words used for the search were cancer, tumor, malignancy, pain, neuropathic pain, patient, physician, oncology, barriers, pain management, pain control, opioid, and analgesia. The last search was carried out in June 2013. Only articles in English were considered, and original reports, review articles, guidelines, meta-analyses, systematic reviews, editorials, commentaries, and letters were included. Articles in languages other than English and case reports were excluded.
BARRIERS TO CANCER PAIN MANAGEMENT FROM THE PERSPECTIVE OF PHYSICIANS
The undermedication of cancer pain is a common unsolved problem in the management of patients with cancer, and physicians seem to be aware of this problem. Most physicians who participated in survey-based studies reported that patients with cancer were undermanaged, and this perception remained mostly unchanged over time but varied greatly by geographic region. In 1990, 86% of US physicians who participated in a survey conducted by the Eastern Cooperative Oncology Group (ECOG) reported that many patients with cancer were undermanaged,17 and 7 years later, 83% of the members of the radiation oncology therapy group still believed that patients were undertreated for pain.18 In Israel in the mid 1990s, 58% of physicians believed that cancer pain could be managed in more than 75% of patients, but only 17% reported that they were capable of achieving this target in their own practice.19 More recently, approximately half of Finnish physicians believed that cancer pain was well managed in their practice (47% of oncologists and 61% of other physicians),20 and more than half of a group of French physicians surveyed (including 51% of oncologists and 60% of primary care physicians) were satisfied with cancer pain management in their country.21 Physician-related reasons for the undermedication of cancer pain have been studied. The majority of these studies either asked physicians to select from a list of barriers or provided open-ended questions. Although variation exists among the studies, frequently reported barriers included poor pain assessment, a lack of knowledge among staff, a reluctance of physicians to prescribe opioids, legal or administrative constraints, a reluctance of patients to take opioids, and a reluctance of patients to report their pain (Table 1). 1728
© 2014 by American Society of Clinical Oncology
Table 1. Barriers to Cancer Pain Management From the Perspective of Professionals Barrier Related to professional Poor pain assessment Lack of knowledge Reluctance to prescribe opioids Fear of adverse effects Risk of tolerance Fear of drug addiction Fear of legal/administrative constraints Excessive regulation of opioids at pharmacy Perception that nonopioid analgesics have same efficacy as opioid analgesics Perception of negative public image of morphine Nursing staff reluctance to administer opioids Discrepancy between self-evaluation and knowledge Lack of specialists Related to patient Patient reluctance to report pain Patient reluctance to take opioids Patient inability to pay for analgesics Related to health care system Lack of neurodestructive procedures Lack of psychosocial support services Lack of equipment or skills Lack of access to wide range of analgesics Lack of access to professional methods Difficulty in accessing services to enable nonpharmacologic pain management Impact of distance on ability to access pain-related services Lack of coordination across multiple providers Difficulty in accessing interventional pain services Lack of support from specialist in pain and palliative care Inadequate guidance of pain specialist Lack of access to wide range of opioids Lack of staff time to attend to pain needs of patient
Poor Pain Assessment Inadequate assessment of pain is the barrier to cancer pain management that has been most frequently mentioned by physicians.17-20,22 The expression of pain by patients is the only source of information for pain evaluation. Use of standardized pain assessment tools allows clinicians to assess this subjective symptom in a reliable and valid manner. The visual analog scale (VAS) and NRS are simple and easy to use; however, only 7% to 43% of physicians use one of these scales in their practice, and multidimensional questionnaires are rarely used.20,23-25 Alarmingly, 30% to 51% of physicians thought that patients exaggerated their pain to attract attention.26 Moreover, only a small number of physicians reported applying pain management guidelines in their practice.19,23 Physicians’ Reluctance to Administer Opioids The literature shows that 23% to 31% of physicians tended to delay strong opioids until patients reached the terminal phase of their disease or until their pain became intractable. This reluctance to use opioids was higher among primary care physicians than among oncologists,17,18,21,27,28 and oncologists rated their peers as being more conservative in terms of the prescription of opioids.22 In cases of severe JOURNAL OF CLINICAL ONCOLOGY
Information downloaded from jco.ascopubs.org and provided by at Univ of Texas Libraries on June 1, 2014 from Copyright © 2014 American Society of Clinical Oncology. All rights reserved. 128.83.63.20
Overcoming Barriers in Cancer Pain Management
cancer pain, only approximately half of physicians chose to treat using strong opioids.17,18,26 A number of physician characteristics were related to the early aggressive management of cancer pain: recent training, use of VAS or NRS for pain evaluation, less fear of addiction, self-evaluation as a medical oncologist (v non–medical oncologist), viewing pain relief as a goal of treatment, seeing themselves as liberal in pain management, and attributing patient requests to elevate dosage to increased pain rather than addiction.17,24 Lack of Knowledge Investigations into physician knowledge of cancer pain management have been conducted in various ways, from asking questions on the concepts of guidelines to asking detailed questions based on clinical conditions. Oncologists showed a greater basic knowledge of cancer pain management than did other specialists (eg, general practitioners, internal medicine specialists, and geriatric specialists); however, more than half of oncologists failed to correctly answer questions based on case scenarios.20 With respect to basic knowledge, 13% to 68% of physicians were familiar with the WHO guidelines or other cancer pain management guidelines, but the level of understanding varied among physicians.20,29,30 The following topics have been identified as areas of knowledge deficiency among physicians: regular medication for chronic cancer pain (42%), the pathophysiology of cancer pain (especially neuropathic pain), equianalgesic dose and dose titration, breakthrough pain, adjuvant medications, addiction, and tolerance.19,21,25,28,29,31,32 Discrepancy Between Perception and Reality Physicians reported that cancer pain was poorly managed in clinical practice, and this finding correlates well with reports on the prevalence of undermanaged cancer pain.5,15 Paradoxically, physicians often self-reported that they had a good working knowledge of cancer pain and its management. For example, 78% to 93% of oncologists reported having a strong knowledge of cancer pain, which is higher than the percentage reported by other specialists.18,21,22,31 When tested, oncologists were found to have a good general knowledge (eg, familiarity with WHO guidelines), but they scored poorly when asked about specific clinical situations.20,22 This discrepancy between self-assessment and actual practice indicates that physicians may not fully realize their knowledge deficiencies, which could represent a potential barrier to cancer pain management. Other Barriers to Cancer Pain Management A fear of addiction is one barrier that explains why physicians are reluctant to prescribe opioids. It has been shown that 25% to 40% of physicians worry about addiction, and this rate was higher for patients with a family history of addiction.21,27 The risk of tolerance (requiring ever-higher doses of opioids), requirement for opioid prescriptions to be written on special prescription forms, and negative perception of opioids were some of the key barriers for physicians.19,21,29,33 In terms of its role as a barrier to cancer pain management, the fear of regulation is experienced quite differently in China compared with other countries. Approximately 75% of Chinese physicians stated that excessive state regulation of opioid prescription was one of the major barriers to cancer pain management, whereas 8% to 27% of physicians in Western countries described this factor as a barrier to cancer pain management.17-21,23,26,28,29,33 Regulatory constraints on opioid prescription differ widely among countries, with physicians in www.jco.org
developed countries having access to a wide range of opioids and those in developing countries having limited treatment options. Surveys of US medical oncologist in 2009 and of Australian oncologists in 2011 and 2012 revealed that a majority of physicians did not refer patients to pain or palliative care specialists because of difficulties in accessing or scheduling appointments with these services.22,23 Interventions to Address Professional Barriers to Cancer Pain Management Intervention studies to improve cancer pain management on the professional side included professional education, pain assessment, and consultation with a specialist. Professional intervention for nurses has been reported to improve the knowledge and attitude of the nurses after education; however, no study has shown that this improvement in knowledge results in an improvement in pain management.34-36 Schmerz-Therapie in der Onkologischen Paediatrie (STOP), a nationwide quality improvement program on pediatric oncology pain control from 1997 to 2001 in Germany, showed promising results for improving knowledge and practice.37 This study compared pain management in pediatric oncology practices between active quality management (QM) departments and nonactive QM departments. Both study arms received training and a manual based on contemporary pain practices, and the active QM departments also had in-depth training and periodic feedback. Eight departments (36 participants) were enrolled in the active QM arm, and 64 departments (193 participants) were enrolled in the nonactive QM arm. The participants included head physicians, ward physicians, head nurses, and psychologists/social workers. Active QM departments showed improvements in the knowledge of pain control and neuropathic pain among health care professionals, including the use of less painful modes of administration and a reduction in the usage of mixed opioid agonists-antagonists in their practice. Patients between ages 12 and 17 years and parents of patients younger than age 12 years in the active QM arm indicated decreased pain intensity and decreased incidence of severe pain. According to the participant self-assessments, STOP improved practical pain management in the active QM departments, whereas the change was negligible in the nonactive QM departments. ECOG also conducted a study to compare the effectiveness of a standardized analgesic protocol for cancer pain management versus leaving pain management to the discretion of the treating physician. In a group of patients with lung or prostate cancer, the proportion of pain reduction of the worst pain was higher in the analgesic protocol group than in the physician discretion group at 2-week follow-up (48% v 15%; P ⬍ .001), and this difference was maintained 4 weeks later (52% v 19%; P ⫽ .045). The worst pain was reduced by 27% in the analgesic protocol group. Although the study was closed early because of poor accrual, the analgesic protocol group exhibited better pain control.38 BARRIERS TO CANCER PAIN MANAGEMENT FROM THE PERSPECTIVE OF PATIENTS
Cognitive barriers, affective barriers, and nonadherence to pain medication represent some common patient-related factors that can decrease the effectiveness of cancer pain management (Table 2). © 2014 by American Society of Clinical Oncology
Information downloaded from jco.ascopubs.org and provided by at Univ of Texas Libraries on June 1, 2014 from Copyright © 2014 American Society of Clinical Oncology. All rights reserved. 128.83.63.20
1729
Jung Hye Kwon
Table 2. Barriers to Pain Management From the Perspective of Patients Barrier Cognitive Concern regarding disease progression Concern regarding addiction Concern over development of tolerance Adverse effects Idea of being a good patient Fatalistic belief regarding cancer pain Concern about distracting physician from cancer care Fear of injections Harmful for immune system Affective Adherence to medication
Cognitive Barriers to Cancer Pain Management Because pain is a subjective symptom, a patient’s attitude toward and knowledge of cancer pain and its management may influence pain assessment and its related outcomes. A patient who has concerns and misconceptions about pain medications be reluctant to report pain and take opioids. Other potential barriers from the patient perspective may include miscommunication with physicians (under-reporting of symptoms to avoid distracting physician from providing cancer treatments), misconceptions regarding pain medicine (fear of adverse effects, addiction, tolerance, and lowered immunity caused by pain medicine), and fatalistic beliefs (inevitably, uncontrollability, and idea that increasing pain indicates disease progression). These patientrelated barriers to cancer pain management have been studied using a 27-item self-reported questionnaire developed specifically for the purpose and then subsequently modified to generate the Barriers Questionnaire II.39,40 Patient-related barriers to cancer pain management can be associated with poor quality of life, poor pain control according to a pain management index (calculated by subtracting pain intensity score [none, 0; mild, 1; moderate, 2; severe, 3] from analgesic usage score [0, no analgesics; 1, nonopioid analgesics; 2, weak opioids; 3, strong opioids], with negative score indicating inadequate management), and negative mood (ie, depression).39-41 Patient-related barriers to cancer pain management vary among cultures. According to a meta-analysis by Chen et al,42 Asian patients perceived greater barriers to managing cancer pain than did Western patients, particularly with respect to concerns about disease progression, tolerance, and fatalism. Affective Barriers to Cancer Pain Management Psychological distress has been shown to be significantly associated with the perception of pain.43 Higher pain intensity was associated with a higher level of psychological distress, including depression, anxiety, hostility, mood disturbances, and anger.44 Our recent study on patient-reported barriers to cancer pain management in oncology clinics revealed that higher scores on the Beck Depression Inventory were associated with higher scores on the Barriers Questionnaire II in a multivariable regression analysis.41 A study by Wang et al45 suggested that a greater improvement of depression was one of the predictors of cancer-related pain improvement over time. Testing positive with regard to depression 1730
© 2014 by American Society of Clinical Oncology
according to the Patient Health Questionnaire–2 was also reported to be associated with poorer medication adherence in patients with advanced lung cancer.46 Given the importance of psychological well-being in pain management, routine screening for depression and anxiety should be part of initial pain assessment. Adherence to Pain Medications Adherence to pain medication was also related to the outcome of pain management. Adherence to regular opioids was reported to be 63% to 91%, and adherence to as-needed medications was reported to be 22% to 27%.47-49 In a study of Taiwanese outpatients with cancer, negative beliefs regarding opioid analgesics were associated with low opioid adherence (r ⫽ ⫺0.3; P ⬍ .01). Furthermore, the opioid-taking self-efficacy of patients (self-efficacy defined as belief or confidence in one’s capability to carry out a certain behavior to produce a desired outcome) was positively correlated with opioid adherence (r ⫽ 0.22; P ⬍ .05) and pain relief (r ⫽ 0.35; P ⬍ .01). The opioid-taking self-efficacy of patients was the only significant predictor of pain relief in a hierarchic multiple regression analysis that included sex, education, and beliefs about analgesics as independent factors (explaining 11% of variance; P ⫽ .001).47 Another study of patients with cancer revealed that better adherence to provider-recommended treatments was associated with less-severe pain.48 Regular follow-up appointments to assess adherence to analgesic medication are important to achieve good pain management. The cost of opioids also varies by country, and some patients have difficulty paying for their prescriptions.50 Interventions to Address Patient-Related Barriers to Cancer Pain Management Patient-based educational interventions have been postulated to facilitate better cancer pain management through changes in knowledge, attitudes, and beliefs. A meta-analysis of 21 randomized trials by Bennett et al51 was conducted to determine the effects of various interventions on cancer pain management. Patient education had a positive effect on patient knowledge of cancer pain management (P ⫽ .008) and resulted in a statistically significant reduction in average pain intensity (0 to 10 NRS from the Brief Pain Inventory), with a 1.1-point reduction in the worst pain experienced by patients. However, the intervention showed no significant effects on mood or quality of life. Most of the interventions consisted of face-to-face coaching sessions (15 to 60 minutes) with an informational booklet. No consistent effects were detected regarding medication adherence or self-efficacy. This study suggested that intervention has modest effects on pain intensity, attitude, and knowledge relative to usual care based on the results of the meta-analysis. A recent randomized controlled trial52 of a tailored education and coaching (TEC) intervention was conducted in patients with cancer with moderate pain and functional impairment in an attempt to enhance the management of cancer-related pain through patient education and coaching. Communication self-efficacy was improved in the TEC group (P ⬍ .001). However, pain misconceptions decreased in both groups, and no statistically significant difference was detected; pain misconceptions were significantly reduced to a similar degree in both groups (P ⬍ .001). Improvement in pain-related impairment (⫺0.25 points on 5-point scale; 95% CI, ⫺0.43 to ⫺0.06; JOURNAL OF CLINICAL ONCOLOGY
Information downloaded from jco.ascopubs.org and provided by at Univ of Texas Libraries on June 1, 2014 from Copyright © 2014 American Society of Clinical Oncology. All rights reserved. 128.83.63.20
Overcoming Barriers in Cancer Pain Management
P ⫽ .01) in the TEC group was only observed at the 2-week follow-up, but this improvement was not sustained at 6 or 12 weeks. TEC had no significant effect on the reduction of pain severity or improvement in functional status or well-being. There is good evidence to support the role of patient education in cancer pain management. However, there is wide variation among existing interventions, making it difficult to provide a specific recommendation in the absence of data that can be used to make direct comparisons. Future studies should examine the optimal components of patient education and identify the most effective program. BARRIERS TO CANCER PAIN MANAGEMENT FROM SYSTEMIC PERSPECTIVES
Barriers Related to Opioids The range of available drugs and accessibility of opioids for cancer pain vary according to country. Physicians in developed countries may experience fewer constraints from legal or regulatory bodies, whereas those who practice in developing countries often have to deal with more restrictions on opioid prescriptions. Less than 50% of physicians in France, Canada, and the United States felt that prescribing opioids was inconvenient or that their opioid prescriptions for cancer pain were influenced by regulation, whereas more than 70% of Chinese physicians perceived a limitation on their ability to prescribe opioids because of strong regulation.17,29-31 However, even US physicians have misconceptions about regulatory monitoring; for example, almost 50% of physicians surveyed were concerned that too many narcotic prescriptions would lead to utilization reviews by a regulatory agency.27 Barriers Related to the Health Care System Multidimensional pain control requires collaboration with other specialists, especially palliative care physicians. Surveys of physicians revealed barriers to the access of pain and palliative care specialists.17,18,23 Physicians reported difficulty accessing other health care professionals, including specialists in neurodestructive procedures (5% to 31%), interventional pain services (88%), psychosocial support (11% to 54%), and nonpharmacologic pain management (88%). Some physicians perceived difficulty accessing specialists because of the physical distance between their practice and the specialist services.17,18,23,28,33 Barriers Related to Education A majority of physicians surveyed reported that education on cancer pain management during medical school and residency training was poor and that more extensive training was necessary in Denmark,53 Finland,20 France,21 Israel,19 South Korea,26 Sweden,25 Taiwan,28 China,29 and the United States.17 Of the participants, 10% to 19% (n ⫽ 879) were satisfied with their pain-related education during medical school, and 52% to 67% rated it as poor.17,19,53 More than half of physicians reported that they had not received training in cancer pain management.21 The evaluation of pain education was better for physicians who had received education and training recently than for older physicians with regard to both medical school and residency training (P ⫽ .01).22 Only 20% to 25% hematology-oncology fellows completed a mandatory palliative care rotation during their www.jco.org
fellowship,54 and education on pain management remained limited even for these trainees.55
STRATEGIES TO OVERCOME BARRIERS TO CANCER PAIN MANAGEMENT
Cancer pain is a multidimensional symptom with both physical and nonphysical components. Adequate pain control requires a multidimensional approach toward assessment and management. Barriers to cancer pain management are also multidimensional in nature and include patient-, physician-, and system-related factors. Successful management of cancer pain therefore mandates multidisciplinary interventions by interprofessional teams.56-58 The following list of recommendations may help address some common barriers to cancer pain management.59-61 Assessment of pain and outcome ● Using validated pain tools for screening and monitoring (eg, NRS and VAS) ● Providing multidimensional evaluation, including physical, functional, psychosocial, and spiritual aspects (eg, Edmonton Symptom Assessment System or Edmonton Classification System for Cancer Pain) ● Evaluating comorbidities ● Ongoing assessment of pain with regular follow-up appointments Management of cancer pain ● Abiding by current updated guidelines (eg, WHO guidelines, NCCN guidelines, and American Pain Society guidelines) ● Choosing appropriate analgesics with adequate dosages, routes, and schedules ● Choosing adequate adjuvant analgesics according to pain pathophysiology ● Monitoring the outcome after starting analgesics ● Anticipating and treating analgesic adverse effects ● Collaborating with other specialties, especially palliative care physicians, for a multidisciplinary approach Education of patients and family members ● Informing patients that most cancer pain can be alleviated, while also setting realistic expectations and pain goals ● Providing psychosocial support ● Providing patient and family caregiver education on the appropriate use of pain medications ● Providing patients with pain and medication diaries Education of physicians and health care professionals ● Didactic lectures and rotations on pain management and palliative care for students and trainees ● Continuing medical education on pain topics for practicing clinicians ● Interdisciplinary pain management rounds to discuss patient cases ● Increased training of pain and palliative care specialists Overcoming system-based issues ● Advocacy for increased availability to opioids in countries with limited access ● Increase availability of pain and palliative care services © 2014 by American Society of Clinical Oncology
Information downloaded from jco.ascopubs.org and provided by at Univ of Texas Libraries on June 1, 2014 from Copyright © 2014 American Society of Clinical Oncology. All rights reserved. 128.83.63.20
1731
Jung Hye Kwon
DISCUSSION
Cancer pain is a multidimensional symptom that is frequently undermanaged. Barriers to cancer management have many facets, including patients, health care providers, and the system. This multifaceted nature of barriers in cancer pain management might be the reason for the failure of most one-sided barrier-approach studies. A multidirectional interdisciplinary approach might be the best way to improve cancer pain management by overcoming REFERENCES 1. Yamagishi A, Morita T, Miyashita M, et al: Pain intensity, quality of life, quality of palliative care, and satisfaction in outpatients with metastatic or recurrent cancer: A Japanese, nationwide, regionbased, multicenter survey. J Pain Symptom Manage 43:503-514, 2012 2. Koyyalagunta D, Bruera E, Solanki DR, et al: A systematic review of randomized trials on the effectiveness of opioids for cancer pain. Pain Physician 15:ES39-ES58, 2012 (suppl 3) 3. Valdimarsdo´ttir U, Helgason AR, Fu¨rst CJ, et al: The unrecognised cost of cancer patients’ unrelieved symptoms: A nationwide follow-up of their surviving partners. Br J Cancer 86:1540-1545, 2002 4. Breivik H, Cherny N, Collett B, et al: Cancerrelated pain: A pan-European survey of prevalence, treatment, and patient attitudes. Ann Oncol 20: 1420-1433, 2009 5. van den Beuken-van Everdingen MH, de Rijke JM, Kessels AG, et al: Prevalence of pain in patients with cancer: A systematic review of the past 40 years. Ann Oncol 18:1437-1449, 2007 6. van den Beuken-van Everdingen MH, de Rijke JM, Kessels AG, et al: High prevalence of pain in patients with cancer in a large population-based study in the Netherlands. Pain 132:312-320, 2007 7. World Health Organization: Cancer Pain Relief. Geneva, Switzerland, World Health Organization, 1986 8. National Comprehensive Cancer Network: NCCN clinical practice guidelines in oncology. http:// www.nccn.org/professionals/physician_gls/ f_guidelines.asp#supportive 9. Caraceni A, Hanks G, Kaasa S, et al: Use of opioid analgesics in the treatment of cancer pain: Evidence-based recommendations from the EAPC. Lancet Oncol 13:e58-e68, 2012 10. Takeda F: Results of field-testing in Japan of the WHO draft interim guidelines on relief of cancer pain. http://apps.who.int/iris/handle/10665/60895? mode⫽full&submit_simple⫽Show⫹full⫹item⫹record 11. Ventafridda V, Tamburini M, Caraceni A, et al: A validation study of the WHO method for cancer pain relief. Cancer 59:850-856, 1987 12. Walker VA, Hoskin PJ, Hanks GW, et al: Evaluation of WHO analgesic guidelines for cancer pain in a hospital-based palliative care unit. J Pain Symptom Manage 3:145-149, 1988 13. Zech DF, Grond S, Lynch J, et al: Validation of World Health Organization guidelines for cancer pain relief: A 10-year prospective study. Pain 63:65-76, 1995 14. Cleeland CS, Gonin R, Hatfield AK, et al: Pain and its treatment in outpatients with metastatic cancer. N Engl J Med 330:592-596, 1994 15. Deandrea S, Montanari M, Moja L, et al: Prevalence of undertreatment in cancer pain: A 1732
© 2014 by American Society of Clinical Oncology
barriers. Moreover, pain management education should be provided to physicians throughout medical school, residency, fellowship, and practice.
AUTHOR’S DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST The author(s) indicated no potential conflicts of interest.
review of published literature. Ann Oncol 19:19851991, 2008 16. Hong SH, Roh SY, Kim SY, et al: Change in cancer pain management in Korea between 2001 and 2006: Results of two nationwide surveys. J Pain Symptom Manage [epub ahead of print on September 24, 2010] 17. von Roenn JH, Cleeland CS, Gonin R, et al: Physician attitudes and practice in cancer pain management: A survey from the Eastern Cooperative Oncology Group. Ann Intern Med 119:121-126, 1993 18. Cleeland CS, Janjan NA, Scott CB, et al: Cancer pain management by radiotherapists: A survey of radiation therapy oncology group physicians. Int J Radiat Oncol Biol Phys 47:203-208, 2000 19. Sapir R, Catane R, Strauss-Liviatan N, et al: Cancer pain: Knowledge and attitudes of physicians in Israel. J Pain Symptom Manage 17:266-276, 1999 20. Silvoniemi M, Vasankari T, Vahlberg T, et al: Physicians’ self-assessment of cancer pain treatment skills: More training required. Support Care Cancer 20:2747-2275, 2012 21. Larue F, Colleau SM, Fontaine A, et al: Oncologists and primary care physicians’ attitudes toward pain control and morphine prescribing in France. Cancer 76:2375-2382, 1995 22. Breuer B, Fleishman SB, Cruciani RA, et al: Medical oncologists’ attitudes and practice in cancer pain management: A national survey. J Clin Oncol 29:4769-4775, 2011 23. Luckett T, Davidson PM, Boyle F, et al: Australian survey of current practice and guideline use in adult cancer pain assessment and management: Perspectives of oncologists. Asia Pac J Clin Oncol [epub ahead of print on December 17, 2012] 24. Yun YH, Park SM, Lee K, et al: Predictors of prescription of morphine for severe cancer pain by physicians in Korea. Ann Oncol 16:966-971, 2005 25. Rawal N, Hylander J, Arne´r S: Management of terminal cancer pain in Sweden: A nationwide survey. Pain 54:169-179, 1993 26. Kim MH, Park H, Park EC, et al: Attitude and knowledge of physicians about cancer pain management: Young doctors of South Korea in their early career. Jpn J Clin Oncol 41:783-791, 2011 27. Weinstein SM, Laux LF, Thornby JI, et al: Physicians’ attitudes toward pain and the use of opioid analgesics: Results of a survey from the Texas Cancer Pain Initiative. South Med J 93:479487, 2000 28. Ger LP, Ho ST, Wang JJ: Physicians’ knowledge and attitudes toward the use of analgesics for cancer pain management: A survey of two medical centers in Taiwan. J Pain Symptom Manage 20:335344, 2000 29. Yanjun S, Changli W, Ling W, et al: A survey on physician knowledge and attitudes towards clinical use of morphine for cancer pain treatment in China. Support Care Cancer 18:1455-1460, 2010
30. Wolfert MZ, Gilson AM, Dahl JL, et al: Opioid analgesics for pain control: Wisconsin physicians’ knowledge, beliefs, attitudes, and prescribing practices. Pain Med 11:425-434, 2010 31. Gallagher R, Hawley P, Yeomans W: A survey of cancer pain management knowledge and attitudes of British Columbian physicians. Pain Res Manag 9:188-194, 2004 32. Larue F, Colleau SM, Brasseur L, et al: Multicentre study of cancer pain and its treatment in France. BMJ 310:1034-1037, 1995 33. Yu S, Wan XS, Cheng Y, et al: Special aspects of cancer pain management in a Chinese general hospital. Eur J Pain 5:15-20, 2001 (suppl A) 34. Huth MM, Gregg TL, Lin L: Education changes Mexican nurses’ knowledge and attitudes regarding pediatric pain. Pain Manag Nurs 11:201208, 2010 35. Ger LP, Chang CY, Ho ST, et al: Effects of a continuing education program on nurses’ practices of cancer pain assessment and their acceptance of patients’ pain reports. J Pain Symptom Manage 27:61-71, 2004 36. Vallerand AH, Riley-Doucet C, Hasenau SM, et al: Improving cancer pain management by homecare nurses. Oncol Nurs Forum 31:809-816, 2004 37. Zernikow B, Hasan C, Hechler T, et al: Stop the pain! A nation-wide quality improvement programme in paediatric oncology pain control. Eur J Pain 12:819-833, 2008 38. Cleeland CS, Portenoy RK, Rue M, et al: Does an oral analgesic protocol improve pain control for patients with cancer? An intergroup study coordinated by the Eastern Cooperative Oncology Group. Ann Oncol 16:972-980, 2005 39. Ward SE, Goldberg N, Miller-McCauley V, et al: Patient-related barriers to management of cancer pain. Pain 52:319-324, 1993 40. Gunnarsdottir S, Donovan HS, Serlin RC, et al: Patient-related barriers to pain management: The Barriers Questionnaire II (BQ-II). Pain 99:385-396, 2002 41. Kwon JH, Oh SY, Chisholm G, et al: Predictors of high score patient-reported barriers to controlling cancer pain: A preliminary report. Support Care Cancer 21:1175-1183, 2013 42. Chen CH, Tang ST, Chen CH: Meta-analysis of cultural differences in Western and Asian patientperceived barriers to managing cancer pain. Palliat Med 26:206-221, 2012 43. Delgado-Guay M, Parsons HA, Li Z, et al: Symptom distress in advanced cancer patients with anxiety and depression in the palliative care setting. Support Care Cancer 17:573-579, 2009 44. Zaza C, Baine N: Cancer pain and psychosocial factors: A critical review of the literature. J Pain Symptom Manage 24:526-542, 2002 45. Wang HL, Kroenke K, Wu J, et al: Predictors of cancer-related pain improvement over time. Psychosom Med 74:642-647, 2012 JOURNAL OF CLINICAL ONCOLOGY
Information downloaded from jco.ascopubs.org and provided by at Univ of Texas Libraries on June 1, 2014 from Copyright © 2014 American Society of Clinical Oncology. All rights reserved. 128.83.63.20
Overcoming Barriers in Cancer Pain Management
46. Yoong J, Traeger LN, Gallagher ER, et al: A pilot study to investigate adherence to long-acting opioids among patients with advanced lung cancer. J Palliat Med 16:391-396, 2013 47. Liang SY, Yates P, Edwards H, et al: Factors influencing opioid-taking self-efficacy and analgesic adherence in Taiwanese outpatients with cancer. Psychooncology 17:1100-1107, 2008 48. Jerant A, Franks P, Tancredi DJ, et al: Tendency to adhere to provider-recommended treatments and subsequent pain severity among individuals with cancer. Patient Prefer Adherence 5:23-31, 2011 49. Valeberg BT, Miaskowski C, Hanestad BR, et al: Prevalence rates for and predictors of selfreported adherence of oncology outpatients with analgesic medications. Clin J Pain 24:627-636, 2008 50. Dalal S, Bruera E: Access to opioid analgesics and pain relief for patients with cancer. Nat Rev Clin Oncol 10:108-116, 2013
51. Bennett MI, Bagnall AM, Jose´ Closs S: How effective are patient-based educational interventions in the management of cancer pain? Systematic review and meta-analysis. Pain 143:192-199, 2009 52. Kravitz RL, Tancredi DJ, Grennan T, et al: Cancer Health Empowerment for Living without Pain (Ca-HELP): Effects of a tailored education and coaching intervention on pain and impairment. Pain 152:1572-1582, 2011 53. Sjøgren P, Banning AM, Jensen NH, et al: Management of cancer pain in Denmark: A nationwide questionnaire survey. Pain 64:519-525, 1996 54. Hui D, Elsayem A, De la Cruz M, et al: Availability and integration of palliative care at US cancer centers. JAMA 303:1054-1061, 2010 55. Buss MK, Lessen DS, Sullivan AM, et al: Hematology/oncology fellows’ training in palliative
care: Results of a national survey. Cancer 117:43044311, 2011 56. McNeill JA, Sherwood GD, Starck PL: The hidden error of mismanaged pain: A systems approach. J Pain Symptom Manage 28:47-58, 2004 57. Fairchild A: Under-treatment of cancer pain. Curr Opin Support Palliat Care 4:11-15, 2010 59. Zuccaro SM, Vellucci R, Sarzi-Puttini P, et al: Barriers to pain management: Focus on opioid therapy. Clin Drug Investig 32:11-19, 2012 (suppl 1) 60. Green E, Zwaal C, Beals C, et al: Cancerrelated pain management: A report of evidencebased recommendations to guide practice. Clin J Pain 26:449-462, 2010 61. Sun VC, Borneman T, Ferrell B, et al: Overcoming barriers to cancer pain management: An institutional change model. J Pain Symptom Manage 34:359-369, 2007
■ ■ ■
Conquer Cancer Foundation of the American Society of Clinical Oncology The Conquer Cancer Foundation (CCF) was created by foremost cancer physicians of the American Society of Clinical Oncology to seek dramatic advances in the prevention, treatment, and cures of all types of cancer. Working toward the vision of a world free from the fear of cancer, CCF strives to conquer this disease by funding breakthrough cancer research and sharing cutting-edge knowledge with patients and physicians worldwide, by improving quality of and access to care, and by enhancing quality of life for all who are touched by cancer. For more information, visit www.conquercancerfoundation.org.
www.jco.org
© 2014 by American Society of Clinical Oncology
Information downloaded from jco.ascopubs.org and provided by at Univ of Texas Libraries on June 1, 2014 from Copyright © 2014 American Society of Clinical Oncology. All rights reserved. 128.83.63.20
1733
