Several problems may account for the lack of good cancer pain management. Health care professionals may be overly concerned about addiction, the development of analgesic tolerance, side-effect management, and regulatory scrutiny of physicians who prescribe narcotics. They may not be aware of current knowledge concerning the mechanisms of pain and the modalities available for its control. Pain management has had a low priority in cancer care. Similarly, patients have also been concerned about addiction, side effects, and becoming tolerant to analgesics. Patients may also think that pain with cancer is inevitable. As a result, they have been reluctant to report pain or the lack of pain relief as well as to take adequate doses of analgesics [10-13].

In 1990, the Eastern Cooperative Oncology Group [ECOG], a National Cancer Institute supported cooperative group for the development and conduct of cancer-related clinical trials, assessed physicians' attitudes about and knowledge of cancer pain and its control as part of a larger project examining pain management within the group. The specific objectives of this project were 1) to determine the knowledge about cancer pain and its treatment among physicians practicing in ECOG-affiliated institutions; 2) to determine the methods of pain control being used by these physicians; and 3) to compare physician knowledge of and attitudes toward cancer pain and its treatment with the results of a study of cancer pain and its treatment in patients being treated by physicians at these same institutions. The latter study is currently underway throughout the ECOG; this report addresses the first two project objectives.

Methods

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Subjects

We surveyed all ECOG physicians with patient care responsibilities (medical oncologists, hematologists, surgeons, and radiation therapists), practicing in ECOG main institutions, Community Clinical Oncology Program (CCOP) institutions, and Cooperative Group Outreach Program (CGOP) institutions. Of the 1800 surveys sent out to institution data managers, 1177 were returned. Of these, 242 (21%) indicated that they did not wish to participate and 37 (3%) were ineligible (nonphysicians, left ECOG, or did not treat patients) leaving 897 respondents who form the basis of this report. Specialties included internal medicine (64%), surgery (10%), radiation therapy (14%), and other (10%). Subspecialty board certification included medical oncology (44%) and hematology (28%). Collectively, this group of physicians reported that they had treated more than 70 000 cancer patients in the 6 months before the survey. The primary treatment center in which these physicians practiced was best characterized as a comprehensive cancer center for 25% of the physicians, an outpatient treatment center for 27%, a community hospital for 19%, and a teaching hospital for 31%. The median age of the respondents was 42 years (range, 26 to 80 years) and 88% were men.

Questionnaire

We sent a physician cancer pain questionnaire developed by Cleeland and the Pain Research Group at the University of Wisconsin. A smaller physician study using this instrument has been previously reported [14]. The questionnaire was designed to assess physicians' estimates of the magnitude of pain as a specific problem for cancer patients, physicians' attitudes about the adequacy of pain management for cancer pain, and their report of how they manage pain in their own practice setting. As a way of describing more specific pain management practice questions, the questionnaire provided treatment recommendations for a hypothetical patient. Information was also gathered on the physicians' practice setting, training, experience with caring for patients with cancer pain, and personal experience with friends or family members with cancer, persistent pain, or substance abuse. The survey took about 45 minutes to complete.

Statistical Analysis

Descriptive statistics (frequencies, percentages, means, and ranges) for each response are reported. Percentages are reported as whole numbers. Not all respondents answered each question completely; therefore, the numbers that constituted the basis for the analysis of each item are included with the reported responses. For the categorical variables, the Fisher exact test [15] was used to determine candidate variables that were significantly associated with time-to-start, maximum-tolerated opioid analgesic therapy (outcome). The association between continuous predictors and outcome was tested for significance by examining the log-likelihood ratio, chi-square statistic [16]. Differences in mean rankings for barriers to pain control were tested by means of the Mann-Whitney U test [15]. Univariate analyses (two-way associations) were used to initially screen the predictors significantly associated with the outcome variable prognosis (< 6 months versus more than 6 months of the start of maximum opioid analgesic therapy in the treatment of severe pain). Several passes through the data were made to screen variables to obtain the most parsimonious model and at the same time to use as much of the data as possible. The prognostic variables were considered in a multiple logistic regression analysis using stepwise selection. A predictor was considered a candidate if it exhibited marginal association (P 0.25). A F-to-enter probability of 0.25 was therefore used initially and was decreased to 0.05 in the final model. Using this approach, we are confident that strong predictors were not inadvertently excluded from the model. This resulted in eliminating 29 of the 35 possible predictors.

Results

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Concerning the use of analgesics for cancer pain in the United States (n = 864), 86% of the respondents thought that the majority of patients with pain are undermedicated, although 13% thought that most patients receive adequate treatment for pain. Most of the sample (67%) thought that at least 50% of the cancer patients they treat had pain at some point during their illness. Physicians estimated that almost one half of cancer patients (48%) had pain for more than 1 month.

Evaluation of Physician Pain Management Practices

To evaluate individual physician pain management practice, the following hypothetical case scenario was presented:

A 40-year-old man is hospitalized with severe untreated back pain of more than 1-month duration, attributable to bone metastases without vertebral collapse. He weighs 70 kg; he has no cardiovascular or respiratory problems, and his prognosis is more than 24 months. He has no history of medication allergies and is opioid naive. What would be your recommendation for an initial analgesic regimen for this patient? Drug? Dosage? Route?

Most ECOG physicians (93%, n = 882) stated that they would prescribe an opioid analgesic, with 41% indicating a "strong" opioid (morphine or a similar drug), although 51% of physicians chose a "weak" opioid (codeine or an equivalent). Eleven percent prescribed a regimen that also included acetaminophen or an anti-inflammatory agent. Eighty-eight percent chose an oral route of analgesic administration.

In a continuation of the scenario, the patient requests additional pain medication 2 hours before his next dose is due. Physicians were asked to choose an immediate and long-term response to the patient's request. As an immediate response, 68% (n = 876) chose to give the next dose of analgesia and 11% gave a less potent non-narcotic analgesic. No respondent chose to refuse or ignore the patients' request. As a long-term response, 54% (n = 834) chose to change the dosage or interval between doses or both, 23% of physicians chose to change to another analgesic medication, 7% chose to supplement the analgesic prescription with another less potent (non-narcotic) analgesic, and 8% chose to supplement the analgesic prescription with another potent opioid analgesic. Fewer than 1% chose to leave the prescription unchanged. Other choices accounted for the remaining 8% of responses.

The scenario continues,

The patient's pain persists despite palliative radiation therapy to treat the pain. The patient's disease is stable. There are no signs of complications, and he is having no side effects from the medication. What is the most aggressive analgesic drug regimen that you would recommend? Drug? Dose? Route?

Radiotherapy failure was a trigger for more aggressive pain management. At this stage of the scenario, 86% of physicians included a potent opioid (morphine or equivalent) in their pain treatment recommendations, although 11% of physicians recommended a weak opioid. A small number (4% of the sample) continued to recommend an anti-inflammatory agent as their most aggressive analgesic. The oral route of analgesic administration was chosen by 86% (n = 797) of physicians. Prophylactic drugs to manage typical opioid analgesic side effects, such as antiemetics or laxatives, were prescribed by fewer than 1% of the sample.

Respondents were asked: At what disease stage (in terms of prognosis) would you recommend maximum-tolerated narcotic analgesic therapy for treatment of this patient's severe pain? Table 1 presents the responses of the 814 physicians answering this question. Thirty-one percent of respondents reported that they would wait until the patient's prognosis was less than 6 months. The majority of the sample (59%) would prescribe maximum analgesia if the prognosis was less than 24 months, which was the longest prognosis of the possible responses.

We were interested in what respondent characteristics contributed to their choice of when to intervene with maximum-tolerated analgesic therapy, because physicians who wait until advanced disease is present may not be providing adequate relief. As detailed in Methods, the univariate analyses identified 36 possible predictors. The multivariate analyses selected 6 of these predictors as significant, based on complete data for 625 physicians (Table 2). The logistic regression analysis identified characteristics of persons who reported that they would treat pain aggressively earlier in the disease: 1) they tended to be medical oncologists rather than radiation therapists or surgeons, 2) they tended to insist on total pain relief as the goal of treatment, 3) they saw themselves as liberal in pain management compared with colleagues, 4) they were less likely to switch from an oral to an intravenous or intramuscular route of administration, 5) they tended to attribute a terminal patient's request for increased doses of pain medication to an increase in pain, rather than to other reasons [for example, "requesting attention," "anxiety"], and, 6) they reported that their patients had higher levels of pain relief.

Physicians were asked: What hesitation do you have in prescribing more potent analgesics? Of the 714 respondents to this question, 65% acknowledged concerns about the control of side effects as a reason to limit their use of maximum analgesia, although 22% identified concern about building patient tolerance too rapidly as a primary reason for not prescribing more potent analgesia. A small percentage (11%) of physicians did not think that larger doses would increase the effectiveness of their chosen analgesic regimen. Only 2% reported hesitation in prescribing more potent analgesics due to concerns about the possibility of addiction.

Physicians were asked to rank the reasons that formed the basis for their choice of drug therapy for the management of prolonged cancer pain. Thirty-eight percent of 820 respondents based their choice of analgesia on their previous experience in using a drug, although 28% chose drugs on the basis of their relative analgesic potency, and 20% used the patient's analgesic history as an important factor in choosing a particular analgesic therapy. Physicians were asked to rank a list of analgesic medications in terms of their preference for the treatment of prolonged moderate to severe cancer pain, based on their knowledge and experience. A majority (62%, n = 817) rated a strong opioid as their first choice of therapy, although 79% of physicians included a strong opioid among their top three therapy choices. Of those who picked a potent opioid as a first choice, the following medications were chosen: 43%, morphine sulfate-SR (351 of 816); 8%, morphine sulfate-IR (63 of 789); 6%, hydromorphone (48 of 795); 3%, methadone (23 of 787); 2%, levorphanol (15 of 793); and 0.4%, Brompton Cocktail (3 of 817).

Barriers to Pain Control

Only about one half of the sample (51%) believed pain control in their own practice setting was good or very good, (31%) described it as fair, and 18% rated it as poor or very poor. Physicians were asked to rank a list of potential barriers to optimal cancer pain management in terms of how they might impede cancer pain management in his or her setting. Table 3 portrays the percentage of respondents ranking each item as one of the four top barriers. Seventy-six percent (n = 785) of physicians rated poor pain assessment as one of the top four barriers to good pain management. Both patient reluctance to report pain and patient reluctance to take the opioids prescribed were reported to be among the top four by 62% of respondents, and physician reluctance to prescribe medication was reported by 61%.

The response to the barrier question from physicians who practice in states that require multiple-copy prescriptions ("triplicates") for scheduled analgesics (n = 214) was compared with the response from physicians in states without this requirement (n = 552). Concern about regulation was ranked seventh in the triplicate states compared with ninth in nontriplicate states (difference in mean ranking, P = 0.003, Mann-Whitney U test). Physicians in "triplicate states" perceive physician reluctance to prescribe analgesics as a significantly greater barrier to good pain management (rated second) than do physicians in "nontriplicate states" (differences in mean ranking for those rating in the top four, P = 0.002, Mann-Whitney U test).

Education in Pain Management

Only 12% (n = 879) of the sample reported medical school training in cancer pain management as excellent or good. Thirty-six percent reported their training in pain management to be fair, and 52% reported their training to be poor. When asked about pain management training during their residency, only 27% reported this training to be excellent or good. Forty-six percent reported their residency training in cancer pain management to be fair, and 27% reported poor training.

Discussion

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This study, surveying physician members of a large collaborative oncology group, portrays the current status of cancer pain management by oncology specialists and provides data suggesting ways that pain control could be improved. About one half of those sampled rated pain management in their own practice settings to be fair, poor, or very poor. When asked about barriers to good pain management in their own practice setting, most cited poor assessment of pain, patient reluctance to report pain or to take analgesics, and physician reluctance to prescribe analgesics. Physicians practicing in multiple-copy prescription states were more likely to cite physician reluctance to prescribe analgesics and to cite concern about excessive drug regulation as barriers in their setting. A large majority of these oncologic specialists expressed dissatisfaction with their training for pain management in medical school and in residency or fellowship.

In responding to the hypothetical case scenario, almost one third of respondents would wait until the patient's prognosis was 6 months or less before starting maximum-tolerated analgesia for severe pain, and 14% would still not prescribe a morphine-class opioid after failure of a course of palliative radiotherapy. When asked their preference for medications to treat prolonged moderate-to-severe cancer pain, 38% failed to rate a morphine-class opioid as their first-choice therapy. While giving a reasonable portrait of how oncologic specialists manage pain, the survey provides no information on how other physicians, who treat thousands of cancer patients, approach cancer pain control. It is reasonable to assume that many physicians receive even less preparation for pain management than those sampled in this study and would be more reluctant to treat pain aggressively.

Practice and educational changes will be needed before there are significant improvements in cancer pain control. A standard assessment of pain, most often cited by respondents as a barrier to pain management, is rarely a standard component of clinic visits. Failure to appreciate the severity and intensity of the patient's pain can only result in inadequate analgesic prescribing and administration. Without proper assessment, health care providers often underestimate the pain that patients have. One study [17] found no statistically significant correlations between the patients' own pain score and that scored by his or her house officer, nurse, or oncology fellow in patients with pain scores greater than 4 (on a scale of 0 to 10). Often, patients are not even asked about their pain. In one study [18], fewer than one half of medical-surgical inpatients who had pain ever had a member of the health care team ask them about their pain or note the pain in the patient record within the first 72 hours of admission. Numerous methods for assessing pain exist that allow repeated, consistent evaluation by multiple caregivers with little interobserver variability. The routine use of pain assessment tools (for example, the Brief Pain Inventory [19], the Memorial Pain Assessment Card [20], or even a simple 0 to 10 numerical pain severity scale), would enhance patient caregiver communication and improve cancer pain management.

Reporting Pain

Patient reluctance to report pain and to take the analgesics they require for pain management indicates the need for patient education about pain and pain treatment as a part of the routine care of the cancer patient. Without proper assessment, patient reluctance to spontaneously complain of pain becomes a problem of greater magnitude. Patients may not complain of pain because they want to be a "good" patient, may not want to distract the physician from treating the primary disease, may think of pain as an inevitable part of having cancer, or may not want to recognize that their disease is progressing [21]. Many fear that they will loose mental control, become addicted, or have other unmanageable side effects. Many patients also fear that early pain control will preclude pain control later in the disease because of concerns (which their physicians often share) that they will become tolerant to pain medications [22]. Patients need to be assured that pain management is an integral part of their total management and that good pain control can usually be achieved throughout the course of their disease. They need to understand that they need to report their pain and to also report when their pain treatment is no longer working. Routine pain assessment would minimize the effects of patient reluctance to complain of pain.

Patients are often reluctant to take pain medications for many of the same reasons they are reluctant to report that they have pain [22, 23]. Previous studies support the impression of our respondents that patients may not follow prescribed pain treatments. Estimates of noncompliance with or misunderstanding of the instructions for the appropriate use of analgesics for cancer pain management vary from 13% to 57% [23-25]. Patients may chose not to take all of their analgesics because they make an informed decision to balance side effects with pain relief. But patients who do not take analgesics because of misinformation are obviously targets for patient information programs. Patients need to learn that their function can often be significantly improved if their pain is well managed. They need to know that pain medications will not cause them to loose control or become addicted and that they should not deny themselves pain relief because of concerns about becoming tolerant to pain medication. The routine use of written patient educational materials, such as those prepared by the National Cancer Institute and the American Cancer Society, or by the State Cancer Pain Initiatives, can reduce staff time necessary to accomplish these patient education goals.

Prescribing Analgesics

Physician reluctance to prescribe opioid analgesics, which is also identified in this study as a major barrier to adequate pain management, has multiple causes [26]. Our data suggest that this reluctance contributes to considerable variability in the practice of cancer pain management. Part of this variability can be ascribed to the lack of a set of consistent pain management practice principles, including when to use opioid analgesics [27]. This variability might be reduced if practices would adopt one of the existing set of cancer pain management guidelines proposed by the World Health Organization [28], the American Pain Society [29], or the American Medical Association [30]. The Agency for Health Care Policy and Research has just published guidelines for acute and postoperative pain [31] and is developing guidelines for cancer pain management.

Concern about regulatory scrutiny in the prescription of opioid analgesics may also contribute to reluctance to prescribe opioids, as suggested by our study. A survey of Wisconsin physicians found that, due to concerns about regulatory scrutiny, most respondents reduce drug dose or prescription quantity, reduce the number of refills, or choose a drug in a lower schedule [32]. Increased concern about possible diversion of prescribed controlled substances is the product of this society's indignation about the growth of recreational drug use, and there is evidence that multiple-copy prescription laws will spread to additional states. Physicians, who take care of cancer patients in pain, will need to establish a dialogue with drug regulators and medical examining boards to assure that uncontrolled pain in cancer patients is not an unintended product of the war on drugs.

Education in Pain Management

A need for improved training in cancer pain management at all levels of professional education was indicated by the responses to the survey. Although there has been some increase in the space devoted to pain management in textbooks of medicine or oncology, or both, pain management training needs to become a part of the day-to-day clinical evaluation and care of cancer patients. Medical house officers should be able to report the level of their patients' comfort just as they are expected to know the hemoglobin levels or white blood cell counts. If physicians requested pain assessment scores as often as they requested vital signs they would receive an essential lesson in pain management and would give this problem the attention it deserves. Rational prescribing of antibiotics rapidly followed after instruction using structured educational order forms and pocket antibiotic dosing guidelines [33, 34]. Similar methods are likely to be successful for education in the appropriate treatment of pain.

Specific content targets for education were suggested after analyzing the responses to the hypothetical case scenario. Very few respondents considered the use of adjuvant medications. Pain due to bone metastases is the ideal situation for the use of anti-inflammatory agents, yet only 11% of physicians prescribed one as part of their initial treatment regimen. More information about the pharmacology of the opioid analgesics and about opioid side-effect management is needed. A number of respondents would wait until relatively late in the course of the disease to begin maximum-tolerated analgesia or would be hesitant to use morphine or an analgesic of similar potency. One in five respondents were concerned about the development of analgesic tolerance. A majority reported concern about side effects as limiting their opioid prescribing, yet few suggested a plan for side-effect management in their scenario treatment recommendations.

Unfortunately, pain control has historically been a low priority issue in cancer care. Public concern about cancer pain has been one of the major driving forces for legalization of physician-assisted suicide. Despite the fact that, for at least two decades, most major medical journals and the lay media have recognized that many patients have needless pain, this survey of specialists in cancer care suggests that 1) education in pain management remains substandard and, as a result, the practice of pain management is often substandard; 2) communication between physicians and patients about pain continues to be hampered by poor or nonexistent assessment and patient misinformation; and 3) some physicians are still reluctant to use the most effective analgesics and adjuvant medications for pain management. Change will occur only with the concerted and collaborative efforts of health care professionals, policy makers, and patient and family consumers.

Abbreviations

CCOP: Community Clinical Oncology Program

CGOP: Community Group Outreach Program

ECOG: Eastern Cooperative Oncology Group