Background and Methods Pain is often inadequately treated inpatients with cancer. A total of 1308 outpatients with metastaticcancer from 54 treatment locations affiliated with the EasternCooperative Oncology Group rated the severity of their painduring the preceding week, as well as the degree of pain-relatedfunctional impairment and the degree of relief provided by analgesicdrugs. Their physicians attributed the pain to various factors,described its treatment, and estimated the impact of pain onthe patients' ability to function. We assessed the adequacyof prescribed analgesic drugs using guidelines developed bythe World Health Organization, studied the factors that influencedwhether analgesia was adequate, and determined the effects ofinadequate analgesia on the patients' perception of pain reliefand functional status.
Results Sixty-seven percent of the patients (871 of 1308) reportedthat they had had pain or had taken analgesic drugs daily duringthe week preceding the study, and 36 percent (475 of 1308) hadpain severe enough to impair their ability to function. Forty-twopercent of those with pain (250 of the 597 patients for whomwe had complete information) were not given adequate analgesictherapy. Patients seen at centers that treated predominantlyminorities were three times more likely than those treated elsewhereto have inadequate pain management. A discrepancy between patientand physician in judging the severity of the patient's painwas predictive of inadequate pain management (odds ratio, 2.3).Other factors that predicted inadequate pain management includedpain that physicians did not attribute to cancer (odds ratio,1.9), better performance status (odds ratio, 1.8), age of 70years or older (odds ratio, 2.4), and female sex (odds ratio,1.5). Patients with less adequate analgesia reported less painrelief and greater pain-related impairment of function.
Conclusions Despite published guidelines for pain management,many patients with cancer have considerable pain and receiveinadequate analgesia.
Pain is the most persistent and incapacitating symptom of recurrentor metastatic cancer. A large proportion of patients with metastaticcancer have pain long before the terminal stage of their illness1,2,3,4,5.Pain, even when treated, is often severe enough to impair theirability to function,6,7,8 and health care professionals andpatients both agree that pain is often poorly managed7,9,10.Although guidelines for the management of cancer pain have appeared,11,12,13,14they have not been widely adopted, and there is considerablevariability in the treatment of cancer pain9,10. Because oflimitations in sample size, previous studies have not allowedan 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 managedas compared with those whose pain is poorly managed. We reportthe results of the Outpatient Pain Needs Assessment Survey conductedby the Eastern Cooperative Oncology Group (ECOG). This studywas designed to determine the proportion of patients with cancerwho have substantial pain (pain that impairs function), thetypes of pain treatment received by patients with cancer, andthe characteristics of patients who are at greater risk forundermedication with analgesic drugs.
Methods
Study Subjects
Between October 1990 and September 1991 we studied 1308 consecutiveoutpatients with previously diagnosed recurrent or metastaticcancer. An additional 119 patients were approached but did notparticipate, for the following reasons: 68 patients had insufficienttime to respond or declined to participate, 34 were too illto answer questions, and 17 were unable to comprehend or completethe forms. Patients who had undergone surgery within 30 daysof the study were excluded because of the possibility that post-surgicalrather than disease-related pain was being reported. The patientswere drawn from three types of ECOG-affiliated research settings:12 university cancer centers (267 patients); 12 cooperativegroup outreach programs (382 patients), which are community-basedhospitals and practices; and 30 community clinical oncologyprograms (659 patients), 2 of which were specially designatedcenters whose patients consisted primarily of minorities (165patients). 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) inthe seven days before the study, reported that they took analgesicdrugs on a daily basis, or were identified by their physiciansas having pain at the time of the study.
Study Procedures
To assess the severity and the impact of pain, the patientscompleted the Brief Pain Inventory15 at the time of a regularappointment. The inventory asked patients to rate the worstpain that they had had in the past week on a scale of 0 to 10.Using three additional scales, the patients also rated the mildestpain they had experienced, their average degree of pain, andthe pain they were having at the time of the study. Each scalewas presented as a horizontal row of equidistant numbers from0 to 10, with the words "no pain" at the 0 and "pain as badas you can imagine" at the 10. On the same type of scales, thepatients were also asked to rate how much their pain interferedwith 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 askedto estimate the degree of pain relief that they were receivingfrom their pain treatment (as a percentage), to identify areason a human figure where they had pain, and to estimate the causeof their pain (cancer, its treatment, or unrelated causes).An ECOG pilot study demonstrated that the Brief Pain Inventoryhas appropriate psychometric properties (validity, reliability,and sensitivity) when used in multicenter collaborative groupstudies16.
Each patient's physician was asked to describe the patient'scurrent treatment for pain (drugs, doses, and routes used andnonpharmacologic treatments used), to characterize the patient'scancer, to determine the patient's ECOG performance status,17and to attribute the patient's pain to the patient's disease,treatment, or other medical or psychological causes. These datawere collected after the patient had completed the office visit,so that any adjustments in analgesic therapy made as a resultof the Brief Pain Inventory could be included. The physicianwas also asked to rate on a scale of 0 to 10 the patient's levelof pain control and the degree to which pain was interferingwith activity and sleep. The physician attested to filling outthe 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 moresevere. Everyone has mild pain periodically (and some personsdaily) that interferes only slightly with daily life. As painbecomes more severe, it affects more areas of the patient'sdaily functioning. Previous studies have shown that patientswith cancer who rate their pain severity at the midpoint orabove (5 or higher) on a scale of 0 to 10 report disproportionatelymore functional impairment18. Pain of this severity also affectsstandard health indicators adversely, such as activity and appetite18.For the purposes of this study, we defined patients who ratedtheir worst pain as 5 or higher as having substantial pain.
Index of Pain Management
According to the World Health Organization's guidelines forthe management of pain in cancer,11 such management is consideredadequate when there is congruence between the patient's reportedlevel of pain and the potency of the prescribed analgesic drug(its place on the analgesic ladder). The pain-management indexcompares the most potent analgesic prescribed for a patientwith that patient's reported level of pain19. To construct theindex, we determined which of four levels of analgesic-drugtherapy was the most potent one used: 0, no analgesic drug;1, a non-opioid (e.g., a nonsteroidal antiinflammatory drugor acetaminophen); 2, a weak opioid (e.g., codeine); and 3,a strong opioid (e.g., morphine). We then determined the patient'slevel 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 absenceof pain was scored as 0, mild pain as 1, moderate pain as 2,and severe pain as 3. The pain-management index, computed bysubtracting the pain level from the analgesic level, rangesfrom -3 (a patient with severe pain receiving no analgesic drugs)to +3 (a patient receiving morphine or an equivalent and reportingno pain). Negative scores are considered to indicate inadequateorders for analgesic drugs, and scores of 0 or higher are consideredto be a conservative indicator of acceptable treatment. Thepain-management index measures the health care provider's responseto a patient's pain; for example, pain management is not consideredinadequate if the patient is not compliant in taking medication.The index also takes into account drugs prescribed recentlybut not yet taken. Therefore, patients with severe pain whowere prescribed morphine at the time of the survey are classifiedas adequately treated.
Discrepancies between Patients' and Physicians' Ratings of Pain Severity
Because inadequate assessment of pain has been identified asa potential factor in poor pain management,9,10,20 concordancebetween physician and patient about the severity of pain wasindexed by the discrepancy between the patients' and the physicians'ratings of the extent to which pain was interfering with thepatients' activities. This discrepancy score could range from-10 (complete disagreement: patient rating maximal interference,physician rating no interference) to +10 (physician rating maximalinterference, patient rating no interference).
Statistical Analysis
Not all patients with pain were included in each analysis. Patientswere excluded if their responses or those of their physiciansdid not contain data on the variables required for the calculationof pain intensity, the pain-management index, or predictorsof the index.
We were interested in selecting variables that were stronglyassociated with the adequacy of analgesia. For categorical variables,Fisher's exact test21,22 was used to determine possible predictorsof the pain-management index (with a binary outcome of adequateor inadequate analgesia) as well as to compare pain-relatedvariables according to the site of disease. The associationbetween continuous predictors and the index (treated as theoutcome variable) was tested for significance by calculatingthe log-likelihood ratio chi-square statistic23.
Univariate analyses (two-way associations) were used to screenthe predictors of the pain-management index. Continuous variableswere screened with univariate logistic-regression analysis.Logistic-regression analysis also was used to determine possiblepredictors of the index23. This exploratory analysis was conductedto obtain the most parsimonious model while as many of the dataas possible were used, and it resulted in the elimination of18 of a possible 36 predictors. In addition to the variableof the discrepancy in the severity of pain, the demographiccharacteristics of patients and groups of variables representingdisease status, the cause of pain, and the patient's reportof pain severity and analgesic history were considered candidatepredictors. The prognostic variables were considered in a multiplelogistic-regression analysis with stepwise selection. A predictorwas considered a candidate if it had a marginal association(P 0.25), in agreement with current practice23. A cutoff valueof 0.25 was therefore used initially and was decreased to 0.05in the final model so that strong predictors were not inadvertentlyexcluded. This resulted in the elimination of 11 of the 18 possiblepredictors.
The items on the Brief Pain Inventory assessing the degree ofpain-induced interference with daily life were considered outcomevariables for the pain-management index as a way of assessingthe effects of negative scores on functional status. Since increasingseverity of pain is associated with progressive functional impairment,the worst-pain rating was used as a covariate, and the scoreon the pain-management index as the grouping variable (adequatevs. inadequate analgesia). We first conducted a multivariateanalysis of covariance, relying on the large sample and therobustness of analysis of variance in general24. We then conductedunivariate analyses of covariance to determine which items assessingpain-induced interference with daily life differed significantlyaccording to the score on the pain-management index; the significancelevel was interpreted with Bonferroni's adjustment. All statisticaltests were two-tailed.
Results
Table 1 shows demographic data and data on pain-related variablesaccording to the primary disease site. There were no major differencesin the proportion of patients with pain or disease-related painaccording to disease site. For the total group, 41 percent (531of 1308 patients) had pain attributed by their physician tothe disease process and not to cancer treatment, other diseases,or causes unrelated to cancer (Table 1). Among the patientswith pain, 475 of 769 (62 percent) rated their pain as substantial(a score of 5 or higher).
Table 1. Demographic and Pain-Related Variables According to Disease Site among 871 Patients with Recurrent or Metastatic Cancer and Pain.
Adequacy of Analgesic-Drug Therapy
The pain-management index was computed for all patients withpain. Forty-two percent (250 of the 597 patients for whom wehad complete information) of the patients with pain had negativescores (indicating inadequate analgesia). There was no differencebetween the proportion of patients with pain who had negativescores among the various types of institutions (university cancercenters, 40 percent; community-based settings, 39 percent).The percentage of patients with negative scores was significantlyhigher in community clinical oncology programs that treatedpredominantly 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 morelikely 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 scoreson the pain-management index are shown in Table 2. In additionto the type of population served by the institution (minorityvs. nonminority), several other demographic and disease-relatedvariables predicted the scores. The greater the discrepancybetween physician and patient in judging the degree of pain-inducedinterference with activity, the more likely a negative score.A negative score was also more likely among patients whose painwas not related to cancer, patients who were in the oldest quartileof the sample (70 years or older), patients who were judgedto be less ill (better ECOG performance status), and women (Figure 1).
Figure 1. Percentages 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 indexwere more likely than patients without such scores to reportthat their pain treatment had relieved 50 percent or less oftheir pain in the past week (42 percent vs. 27 percent, P<0.001)and had been effective for shorter periods (3 hours vs. 5 to12 hours, P = 0.04). Negative scores were associated with patients'reports of interference with daily life (P = 0.02). The resultsof the univariate analyses of covariance (with worst pain asthe covariate) are shown in Table 3. Patients with negativescores reported more pain-related interference with work andrelationships and tended to report more interference with walking,mood, and enjoyment of life.
Table 3. Mean Degree of Pain-Induced Interference with Functioning among 597 Patients with Cancer and Pain, According to the Adequacy of Pain Management.
Discussion
This study defined the severity of pain experienced by outpatientswith recurrent or metastatic cancer. Over half the patientshad pain. Of those with pain, the majority (62 percent) hadpain that was severe enough to impair function, despite thefact that most were receiving some treatment for the pain (Table 1).In contrast to some other studies,3,5,25 in this study thepercentage of patients with pain or substantial pain did notvary according to the primary site of cancer. In most patientswith pain (85 percent), the pain was attributed by the physicianto 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 veryconservative one; only the type of the analgesic drug prescribedwas used to compute it. The patients could have been receivingan inadequate dose of an analgesic drug of the appropriate potencyor could have been undermedicated because they were not takingthe drugs prescribed for them. On the basis of the pain-managementindex, 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 minoritieswere three times more likely than nonminority patients to havea negative score. In a recent study, Hispanic patients wereonly half as likely to receive analgesic drugs for long-bonefractures as were patients who were not minorities who weretreated in the same emergency setting26. Black patients arealso 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 patientswho were 70 years of age or older (Figure 1). Patients who wererated as less ill (better ECOG performance status) were alsomore likely to have inadequate analgesia, as were patients whosepain was attributed by their physicians to causes other thancancer. The most powerful additional predictor of the scoreon the pain-management index was the discrepancy between thephysician's and patient's estimate of the severity of the patient'spain (its degree of interference with daily activities). Thislast predictor may explain the influence of some of the othervariables; accurate appraisal of the severity of pain may bemore difficult for patients who are not of the same age, sex,or racial or ethnic background as the treating physician. Patientswho look less ill may also be judged to have less pain. Patientswho received less adequate analgesia reported less and shorterpain relief and more pain-related impairment of function.
These findings are consonant with a recent study of the pain-managementpractices of physicians who practice in the same ECOG institutionsin which this study was done10. In responding to a case scenario,almost one third of respondents reported that they would waituntil the patient had less than six months to live before startingthe maximal tolerated analgesia for severe pain, suggestingthe role of the performance status as a determinant of the adequacyof treatment in the current study. Many of the physicians wereconservative in their analgesic management; 14 percent indicatedthat they would not prescribe a morphine-class opioid for apatient with severe pain, even after a course of palliativeradiotherapy had failed. When asked which medications they preferredto use to treat prolonged moderate-to-severe cancer pain, 38percent did not choose a morphine-class opioid first. This conservativeapproach to pain management is liable to be at least partiallyresponsible for the large percentage of patients with inadequateanalgesic orders. When asked about barriers to good pain managementin their own practice setting, 76 percent cited poor assessmentof pain as a problem -- a finding consistent with the strongpredictive role of the discrepancy between patients' and physicians'assessment of the patients' pain in inadequate analgesia reportedhere.
This study documents wide variability in the quality of paintreatment among patients with cancer. The study included onlypatients treated by cancer subspecialists; patients treatedby those without specialized cancer training may be less welltreated29. The study also identifies those at greatest riskfor poor pain management: older patients and minority patientswho are also at risk for substandard or less aggressive treatmentof cancer27,28,30. Consistent recommendations for the managementof cancer pain (similar to the ones used here to index the adequacyof analgesic-drug therapy) have appeared in several major medicaljournals in the past two decades,11,12,13,14 and new ones havejust been issued by the Agency for Health Care Policy and Research31.Several assessment instruments are available to standardizepain assessment and minimize potential biases in physicians'estimates of the severity of their patients' pain14,32,33. Althoughmultiple factors contribute to the poor management of cancerpain,7,9,10,14 patients should have less pain when it is adequatelyappreciated and treated appropriately.
Supported by grants from the Public Health Service (CA 21115to the Eastern Cooperative Oncology Group and CA 26582 to thePain Research Group), the National Cancer Institute, the NationalInstitutes of Health, and the Department of Health and HumanServices.
We are indebted to Ms. Karen Ryan for assistance in the preparationof 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.
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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 MedicalCenter Oncology Program, Hackensack, N.J.; Brooklyn CCOP, Brooklyn,N.Y.; Case Western Reserve University, Cleveland; Universityof Florida-Gainesville, Gainesville; Fox Chase Cancer Center,Philadelphia; Grady Memorial Hospital, Atlanta; Indiana UniversityMedical Center, Indianapolis; Johns Hopkins Oncology Center,Baltimore; Marshfield Clinic, Marshfield, Wis.; Medical Collegeof Ohio, Toledo; Mercy Hospital, Scranton, Pa.; Methodist HospitalCCOP, Indianapolis; Metro-Minneapolis CCOP, Minneapolis; NewarkInner City CCOP, Newark, N.J.; Northwestern University MedicalCenter, Chicago; University of Pennsylvania Cancer Center, Philadelphia;Rush-Presbyterian-St. Luke's Medical Center, Chicago; Universityof Pretoria, Pretoria, South Africa; Stanford University, Stanford,Calif.; Tufts New England Medical Center Hospital, Boston; NatalieWarren Bryant Cancer Center, Tulsa, Okla.; Twin Tiers CCOP,Binghamton, N.Y.; Vanderbilt University, Nashville; and VermontRegional Cancer Center, Burlington.
Treating Cancer Pain
Karnad A. B., Blansfield H. N., Kilwein J. H., Goodman A. N., Marcus C. S., O'Neill W. M., Chambers E. J., Fallon M. T., Bloomer W. D., Cleeland C. S., Jacox A., Carr D. B., Payne R.
Extract |
Full Text
N Engl J Med 1994;
331:199-201, Jul 21, 1994.
Correspondence
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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. 
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