Original Article
Pain and Its Treatment in Outpatients with Metastatic Cancer
N Engl J Med 1994; 330:592-596March 3, 1994
- Abstract
Background and Methods
Pain is often inadequately treated in patients with cancer. A total of 1308 outpatients with metastatic cancer from 54 treatment locations affiliated with the Eastern Cooperative Oncology Group rated the severity of their pain during the preceding week, as well as the degree of pain-related functional impairment and the degree of relief provided by analgesic drugs. Their physicians attributed the pain to various factors, described its treatment, and estimated the impact of pain on the patients' ability to function. We assessed the adequacy of prescribed analgesic drugs using guidelines developed by the World Health Organization, studied the factors that influenced whether analgesia was adequate, and determined the effects of inadequate analgesia on the patients' perception of pain relief and functional status.
Results
Sixty-seven percent of the patients (871 of 1308) reported that they had had pain or had taken analgesic drugs daily during the week preceding the study, and 36 percent (475 of 1308) had pain severe enough to impair their ability to function. Forty-two percent of those with pain (250 of the 597 patients for whom we had complete information) were not given adequate analgesic therapy. Patients seen at centers that treated predominantly minorities were three times more likely than those treated elsewhere to have inadequate pain management. A discrepancy between patient and physician in judging the severity of the patient's pain was predictive of inadequate pain management (odds ratio, 2.3). Other factors that predicted inadequate pain management included pain that physicians did not attribute to cancer (odds ratio, 1.9), better performance status (odds ratio, 1.8), age of 70 years or older (odds ratio, 2.4), and female sex (odds ratio, 1.5). Patients with less adequate analgesia reported less pain relief and greater pain-related impairment of function.
Conclusions
Despite published guidelines for pain management, many patients with cancer have considerable pain and receive inadequate analgesia.
Media in This Article
Figure 1
Percentages of Patients with Pain and Negative Scores on the Pain-Management Index, According to Age and Sex.Table 1
Demographic and Pain-Related Variables According to Disease Site among 871 Patients with Recurrent or Metastatic Cancer and Pain.Article Activity
- Article
Pain is the most persistent and incapacitating symptom of recurrent or metastatic cancer. A large proportion of patients with metastatic cancer have pain long before the terminal stage of their illness1-5. Pain, even when treated, is often severe enough to impair their ability to function,6-8 and health care professionals and patients both agree that pain is often poorly managed7,9,10. Although guidelines for the management of cancer pain have appeared,11-14 they have not been widely adopted, and there is considerable variability in the treatment of cancer pain9,10. Because of limitations in sample size, previous studies have not allowed an examination of the range of pain treatments currently provided, the degree to which these treatments meet existing guidelines, or the characteristics of patients whose pain is well managed as compared with those whose pain is poorly managed. We report the results of the Outpatient Pain Needs Assessment Survey conducted by the Eastern Cooperative Oncology Group (ECOG). This study was designed to determine the proportion of patients with cancer who have substantial pain (pain that impairs function), the types of pain treatment received by patients with cancer, and the characteristics of patients who are at greater risk for undermedication with analgesic drugs.
Methods
Study Subjects
Between October 1990 and September 1991 we studied 1308 consecutive outpatients with previously diagnosed recurrent or metastatic cancer. An additional 119 patients were approached but did not participate, for the following reasons: 68 patients had insufficient time to respond or declined to participate, 34 were too ill to answer questions, and 17 were unable to comprehend or complete the forms. Patients who had undergone surgery within 30 days of the study were excluded because of the possibility that post-surgical rather than disease-related pain was being reported. The patients were drawn from three types of ECOG-affiliated research settings: 12 university cancer centers (267 patients); 12 cooperative group outreach programs (382 patients), which are community-based hospitals and practices; and 30 community clinical oncology programs (659 patients), 2 of which were specially designated centers whose patients consisted primarily of minorities (165 patients). Of the 1308 patients in the study, 871 (67 percent) reported having pain that differed from everyday kinds of pain (such as those caused by headache, sprains, and toothache) in the seven days before the study, reported that they took analgesic drugs on a daily basis, or were identified by their physicians as having pain at the time of the study.
Study Procedures
To assess the severity and the impact of pain, the patients completed the Brief Pain Inventory15 at the time of a regular appointment. The inventory asked patients to rate the worst pain that they had had in the past week on a scale of 0 to 10. Using three additional scales, the patients also rated the mildest pain they had experienced, their average degree of pain, and the pain they were having at the time of the study. Each scale was presented as a horizontal row of equidistant numbers from 0 to 10, with the words “no pain” at the 0 and “pain as bad as you can imagine” at the 10. On the same type of scales, the patients were also asked to rate how much their pain interfered with such things as their enjoyment of life, level of activity, ability to walk, mood, sleep, work, and relations with others. These scales had the phrases “does not interfere” at the 0 and “interferes completely” at the 10. The patients were also asked to estimate the degree of pain relief that they were receiving from their pain treatment (as a percentage), to identify areas on a human figure where they had pain, and to estimate the cause of their pain (cancer, its treatment, or unrelated causes). An ECOG pilot study demonstrated that the Brief Pain Inventory has appropriate psychometric properties (validity, reliability, and sensitivity) when used in multicenter collaborative group studies16.
Each patient's physician was asked to describe the patient's current treatment for pain (drugs, doses, and routes used and nonpharmacologic treatments used), to characterize the patient's cancer, to determine the patient's ECOG performance status,17 and to attribute the patient's pain to the patient's disease, treatment, or other medical or psychological causes. These data were collected after the patient had completed the office visit, so that any adjustments in analgesic therapy made as a result of the Brief Pain Inventory could be included. The physician was also asked to rate on a scale of 0 to 10 the patient's level of pain control and the degree to which pain was interfering with activity and sleep. The physician attested to filling out the form without reading the patient's responses to the survey.
Classification of Patients with Substantial Pain
Pain has a greater impact on the patient as it becomes more severe. Everyone has mild pain periodically (and some persons daily) that interferes only slightly with daily life. As pain becomes more severe, it affects more areas of the patient's daily functioning. Previous studies have shown that patients with cancer who rate their pain severity at the midpoint or above (5 or higher) on a scale of 0 to 10 report disproportionately more functional impairment18. Pain of this severity also affects standard health indicators adversely, such as activity and appetite18. For the purposes of this study, we defined patients who rated their worst pain as 5 or higher as having substantial pain.
Index of Pain Management
According to the World Health Organization's guidelines for the management of pain in cancer,11 such management is considered adequate when there is congruence between the patient's reported level of pain and the potency of the prescribed analgesic drug (its place on the analgesic ladder). The pain-management index compares the most potent analgesic prescribed for a patient with that patient's reported level of pain19. To construct the index, we determined which of four levels of analgesic-drug therapy was the most potent one used: 0, no analgesic drug; 1, a non-opioid (e.g., a nonsteroidal antiinflammatory drug or acetaminophen); 2, a weak opioid (e.g., codeine); and 3, a strong opioid (e.g., morphine). We then determined the patient's level of pain from the worst-pain score on the Brief Pain Inventory (1 to 3, mild; 4 to 7, moderate; and 8 to 10, severe). The absence of pain was scored as 0, mild pain as 1, moderate pain as 2, and severe pain as 3. The pain-management index, computed by subtracting the pain level from the analgesic level, ranges from -3 (a patient with severe pain receiving no analgesic drugs) to +3 (a patient receiving morphine or an equivalent and reporting no pain). Negative scores are considered to indicate inadequate orders for analgesic drugs, and scores of 0 or higher are considered to be a conservative indicator of acceptable treatment. The pain-management index measures the health care provider's response to a patient's pain; for example, pain management is not considered inadequate if the patient is not compliant in taking medication. The index also takes into account drugs prescribed recently but not yet taken. Therefore, patients with severe pain who were prescribed morphine at the time of the survey are classified as adequately treated.
Discrepancies between Patients' and Physicians' Ratings of Pain Severity
Because inadequate assessment of pain has been identified as a potential factor in poor pain management,9,10,20 concordance between physician and patient about the severity of pain was indexed by the discrepancy between the patients' and the physicians' ratings of the extent to which pain was interfering with the patients' activities. This discrepancy score could range from -10 (complete disagreement: patient rating maximal interference, physician rating no interference) to +10 (physician rating maximal interference, patient rating no interference).
Statistical Analysis
Not all patients with pain were included in each analysis. Patients were excluded if their responses or those of their physicians did not contain data on the variables required for the calculation of pain intensity, the pain-management index, or predictors of the index.
We were interested in selecting variables that were strongly associated with the adequacy of analgesia. For categorical variables, Fisher's exact test21,22 was used to determine possible predictors of the pain-management index (with a binary outcome of adequate or inadequate analgesia) as well as to compare pain-related variables according to the site of disease. The association between continuous predictors and the index (treated as the outcome variable) was tested for significance by calculating the log-likelihood ratio chi-square statistic23.
Univariate analyses (two-way associations) were used to screen the predictors of the pain-management index. Continuous variables were screened with univariate logistic-regression analysis. Logistic-regression analysis also was used to determine possible predictors of the index23. This exploratory analysis was conducted to obtain the most parsimonious model while as many of the data as possible were used, and it resulted in the elimination of 18 of a possible 36 predictors. In addition to the variable of the discrepancy in the severity of pain, the demographic characteristics of patients and groups of variables representing disease status, the cause of pain, and the patient's report of pain severity and analgesic history were considered candidate predictors. The prognostic variables were considered in a multiple logistic-regression analysis with stepwise selection. A predictor was considered a candidate if it had a marginal association (P ≤ 0.25), in agreement with current practice23. A cutoff value of 0.25 was therefore used initially and was decreased to 0.05 in the final model so that strong predictors were not inadvertently excluded. This resulted in the elimination of 11 of the 18 possible predictors.
The items on the Brief Pain Inventory assessing the degree of pain-induced interference with daily life were considered outcome variables for the pain-management index as a way of assessing the effects of negative scores on functional status. Since increasing severity of pain is associated with progressive functional impairment, the worst-pain rating was used as a covariate, and the score on the pain-management index as the grouping variable (adequate vs. inadequate analgesia). We first conducted a multivariate analysis of covariance, relying on the large sample and the robustness of analysis of variance in general24. We then conducted univariate analyses of covariance to determine which items assessing pain-induced interference with daily life differed significantly according to the score on the pain-management index; the significance level was interpreted with Bonferroni's adjustment. All statistical tests were two-tailed.
Results
Table 1Table 1
Demographic and Pain-Related Variables According to Disease Site among 871 Patients with Recurrent or Metastatic Cancer and Pain. shows demographic data and data on pain-related variables according to the primary disease site. There were no major differences in the proportion of patients with pain or disease-related pain according to disease site. For the total group, 41 percent (531 of 1308 patients) had pain attributed by their physician to the disease process and not to cancer treatment, other diseases, or causes unrelated to cancer (Table 1). Among the patients with pain, 475 of 769 (62 percent) rated their pain as substantial (a score of 5 or higher).Adequacy of Analgesic-Drug Therapy
The pain-management index was computed for all patients with pain. Forty-two percent (250 of the 597 patients for whom we had complete information) of the patients with pain had negative scores (indicating inadequate analgesia). There was no difference between the proportion of patients with pain who had negative scores among the various types of institutions (university cancer centers, 40 percent; community-based settings, 39 percent). The percentage of patients with negative scores was significantly higher in community clinical oncology programs that treated predominantly minority patients, primarily blacks and Hispanics, than in the other two settings (59 percent [36 of 61 patients]; P = 0.001 by Fisher's exact test). Minority patients were more likely than nonminority patients to have inadequate analgesia.
Predictors of Scores on the Pain-Management Index
The results of the analysis to identify predictors of the scores on the pain-management index are shown in Table 2Table 2
Predictors of Negative Scores on the Pain-Management Index among 538 Patients with Cancer and Pain.. In addition to the type of population served by the institution (minority vs. nonminority), several other demographic and disease-related variables predicted the scores. The greater the discrepancy between physician and patient in judging the degree of pain-induced interference with activity, the more likely a negative score. A negative score was also more likely among patients whose pain was not related to cancer, patients who were in the oldest quartile of the sample (70 years or older), patients who were judged to be less ill (better ECOG performance status), and women (Figure 1Figure 1Percentages of Patients with Pain and Negative Scores on the Pain-Management Index, According to Age and Sex.).Effects of a Negative Score on the Pain-Management Index
Patients who had negative scores on the pain-management index were more likely than patients without such scores to report that their pain treatment had relieved 50 percent or less of their pain in the past week (42 percent vs. 27 percent, P<0.001) and had been effective for shorter periods (3 hours vs. 5 to 12 hours, P = 0.04). Negative scores were associated with patients' reports of interference with daily life (P = 0.02). The results of the univariate analyses of covariance (with worst pain as the covariate) are shown in Table 3Table 3
Mean Degree of Pain-Induced Interference with Functioning among 597 Patients with Cancer and Pain, According to the Adequacy of Pain Management.. Patients with negative scores reported more pain-related interference with work and relationships and tended to report more interference with walking, mood, and enjoyment of life.Discussion
This study defined the severity of pain experienced by outpatients with recurrent or metastatic cancer. Over half the patients had pain. Of those with pain, the majority (62 percent) had pain that was severe enough to impair function, despite the fact that most were receiving some treatment for the pain (Table 1). In contrast to some other studies,3,5,25 in this study the percentage of patients with pain or substantial pain did not vary according to the primary site of cancer. In most patients with pain (85 percent), the pain was attributed by the physician to cancer and not to coexisting conditions or other causes.
We also examined the adequacy of treatment in these patients. The index of treatment adequacy used in this study was a very conservative one; only the type of the analgesic drug prescribed was used to compute it. The patients could have been receiving an inadequate dose of an analgesic drug of the appropriate potency or could have been undermedicated because they were not taking the drugs prescribed for them. On the basis of the pain-management index, 42 percent of all patients who had pain were undermedicated, and the scores did not vary according to treatment setting, except that patients seen at centers treating primarily minorities were three times more likely than nonminority patients to have a negative score. In a recent study, Hispanic patients were only half as likely to receive analgesic drugs for long-bone fractures as were patients who were not minorities who were treated in the same emergency setting26. Black patients are also likely to receive less adequate treatment for cancer27,28. Other factors were also predictive of inadequate analgesia. Women were more likely to have a negative score, as were patients who were 70 years of age or older (Figure 1). Patients who were rated as less ill (better ECOG performance status) were also more likely to have inadequate analgesia, as were patients whose pain was attributed by their physicians to causes other than cancer. The most powerful additional predictor of the score on the pain-management index was the discrepancy between the physician's and patient's estimate of the severity of the patient's pain (its degree of interference with daily activities). This last predictor may explain the influence of some of the other variables; accurate appraisal of the severity of pain may be more difficult for patients who are not of the same age, sex, or racial or ethnic background as the treating physician. Patients who look less ill may also be judged to have less pain. Patients who received less adequate analgesia reported less and shorter pain relief and more pain-related impairment of function.
These findings are consonant with a recent study of the pain-management practices of physicians who practice in the same ECOG institutions in which this study was done10. In responding to a case scenario, almost one third of respondents reported that they would wait until the patient had less than six months to live before starting the maximal tolerated analgesia for severe pain, suggesting the role of the performance status as a determinant of the adequacy of treatment in the current study. Many of the physicians were conservative in their analgesic management; 14 percent indicated that they would not prescribe a morphine-class opioid for a patient with severe pain, even after a course of palliative radiotherapy had failed. When asked which medications they preferred to use to treat prolonged moderate-to-severe cancer pain, 38 percent did not choose a morphine-class opioid first. This conservative approach to pain management is liable to be at least partially responsible for the large percentage of patients with inadequate analgesic orders. When asked about barriers to good pain management in their own practice setting, 76 percent cited poor assessment of pain as a problem -- a finding consistent with the strong predictive role of the discrepancy between patients' and physicians' assessment of the patients' pain in inadequate analgesia reported here.
This study documents wide variability in the quality of pain treatment among patients with cancer. The study included only patients treated by cancer subspecialists; patients treated by those without specialized cancer training may be less well treated29. The study also identifies those at greatest risk for poor pain management: older patients and minority patients who are also at risk for substandard or less aggressive treatment of cancer27,28,30. Consistent recommendations for the management of cancer pain (similar to the ones used here to index the adequacy of analgesic-drug therapy) have appeared in several major medical journals in the past two decades,11-14 and new ones have just been issued by the Agency for Health Care Policy and Research31. Several assessment instruments are available to standardize pain assessment and minimize potential biases in physicians' estimates of the severity of their patients' pain14,32,33. Although multiple factors contribute to the poor management of cancer pain,7,9,10,14 patients should have less pain when it is adequately appreciated and treated appropriately.
Supported by grants from the Public Health Service (CA 21115 to the Eastern Cooperative Oncology Group and CA 26582 to the Pain Research Group), the National Cancer Institute, the National Institutes of Health, and the Department of Health and Human Services.
We are indebted to Ms. Karen Ryan for assistance in the preparation of the manuscript.
Source Information
From the Pain Research Group, Department of Neurology (C.S.C.), and University of Wisconsin Comprehensive Cancer Center (C.S.C., J.A.S.), Madison; Dana-Farber Cancer Institute, Boston (R.G.); Carle Cancer Center, Urbana, Ill. (A.K.H.); Mayo Clinic, Rochester, Minn. (J.H.E.); New York University Medical Center, New York (R.H.B.); and the University of Rochester Cancer Center, Rochester, N.Y. (K.J.P.).
Address reprint requests to Dr. Cleeland at the Pain Research Group, 1900 University Ave., Madison, WI 53705-4013.
Appendix
The following institutions and community clinical oncology programs (CCOPs) also participated in the study: Albany Medical College, Albany, N.Y.; Albert Einstein College of Medicine, Bronx, N.Y.; Bay Area Tumor Institute CCOP, Oakland, Calif.; Hackensack Medical Center Oncology Program, Hackensack, N.J.; Brooklyn CCOP, Brooklyn, N.Y.; Case Western Reserve University, Cleveland; University of Florida-Gainesville, Gainesville; Fox Chase Cancer Center, Philadelphia; Grady Memorial Hospital, Atlanta; Indiana University Medical Center, Indianapolis; Johns Hopkins Oncology Center, Baltimore; Marshfield Clinic, Marshfield, Wis.; Medical College of Ohio, Toledo; Mercy Hospital, Scranton, Pa.; Methodist Hospital CCOP, Indianapolis; Metro-Minneapolis CCOP, Minneapolis; Newark Inner City CCOP, Newark, N.J.; Northwestern University Medical Center, Chicago; University of Pennsylvania Cancer Center, Philadelphia; Rush-Presbyterian-St. Luke's Medical Center, Chicago; University of Pretoria, Pretoria, South Africa; Stanford University, Stanford, Calif.; Tufts New England Medical Center Hospital, Boston; Natalie Warren Bryant Cancer Center, Tulsa, Okla.; Twin Tiers CCOP, Binghamton, N.Y.; Vanderbilt University, Nashville; and Vermont Regional Cancer Center, Burlington.
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