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Complications at the End of Life in Ovarian Cancer

  • Lisa J. Herrinton
    Correspondence
    Address reprint requests to: Lisa J. Herrinton, PhD, Division of Research, Kaiser Permanente Northern California, 2000 Broadway, Oakland CA 94612, USA.
    Affiliations
    Division of Research (L.J.H., J.A.D.), Kaiser Permanente Northern California, Oakland, California; Henry Ford Health Systems (C.N.-D.), Detroit, Michigan; HealthPartners Research Foundation (S.J.R., J.M.J.), Minneapolis, Minnesota; Center for Health Research, Northwest/Hawaii (M.C.H., D.J.B.), Kaiser Permanente Northwest, Portland, Oregon; and Division of Cancer Prevention and Control (S.S.C.), United States Centers for Disease Control and Prevention, Atlanta, Georgia, USA
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  • Christine Neslund-Dudas
    Affiliations
    Division of Research (L.J.H., J.A.D.), Kaiser Permanente Northern California, Oakland, California; Henry Ford Health Systems (C.N.-D.), Detroit, Michigan; HealthPartners Research Foundation (S.J.R., J.M.J.), Minneapolis, Minnesota; Center for Health Research, Northwest/Hawaii (M.C.H., D.J.B.), Kaiser Permanente Northwest, Portland, Oregon; and Division of Cancer Prevention and Control (S.S.C.), United States Centers for Disease Control and Prevention, Atlanta, Georgia, USA
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  • Sharon J. Rolnick
    Affiliations
    Division of Research (L.J.H., J.A.D.), Kaiser Permanente Northern California, Oakland, California; Henry Ford Health Systems (C.N.-D.), Detroit, Michigan; HealthPartners Research Foundation (S.J.R., J.M.J.), Minneapolis, Minnesota; Center for Health Research, Northwest/Hawaii (M.C.H., D.J.B.), Kaiser Permanente Northwest, Portland, Oregon; and Division of Cancer Prevention and Control (S.S.C.), United States Centers for Disease Control and Prevention, Atlanta, Georgia, USA
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  • Mark C. Hornbrook
    Affiliations
    Division of Research (L.J.H., J.A.D.), Kaiser Permanente Northern California, Oakland, California; Henry Ford Health Systems (C.N.-D.), Detroit, Michigan; HealthPartners Research Foundation (S.J.R., J.M.J.), Minneapolis, Minnesota; Center for Health Research, Northwest/Hawaii (M.C.H., D.J.B.), Kaiser Permanente Northwest, Portland, Oregon; and Division of Cancer Prevention and Control (S.S.C.), United States Centers for Disease Control and Prevention, Atlanta, Georgia, USA
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  • Donald J. Bachman
    Affiliations
    Division of Research (L.J.H., J.A.D.), Kaiser Permanente Northern California, Oakland, California; Henry Ford Health Systems (C.N.-D.), Detroit, Michigan; HealthPartners Research Foundation (S.J.R., J.M.J.), Minneapolis, Minnesota; Center for Health Research, Northwest/Hawaii (M.C.H., D.J.B.), Kaiser Permanente Northwest, Portland, Oregon; and Division of Cancer Prevention and Control (S.S.C.), United States Centers for Disease Control and Prevention, Atlanta, Georgia, USA
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  • Jeanne A. Darbinian
    Affiliations
    Division of Research (L.J.H., J.A.D.), Kaiser Permanente Northern California, Oakland, California; Henry Ford Health Systems (C.N.-D.), Detroit, Michigan; HealthPartners Research Foundation (S.J.R., J.M.J.), Minneapolis, Minnesota; Center for Health Research, Northwest/Hawaii (M.C.H., D.J.B.), Kaiser Permanente Northwest, Portland, Oregon; and Division of Cancer Prevention and Control (S.S.C.), United States Centers for Disease Control and Prevention, Atlanta, Georgia, USA
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  • Jody M. Jackson
    Affiliations
    Division of Research (L.J.H., J.A.D.), Kaiser Permanente Northern California, Oakland, California; Henry Ford Health Systems (C.N.-D.), Detroit, Michigan; HealthPartners Research Foundation (S.J.R., J.M.J.), Minneapolis, Minnesota; Center for Health Research, Northwest/Hawaii (M.C.H., D.J.B.), Kaiser Permanente Northwest, Portland, Oregon; and Division of Cancer Prevention and Control (S.S.C.), United States Centers for Disease Control and Prevention, Atlanta, Georgia, USA
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  • Steven S. Coughlin
    Affiliations
    Division of Research (L.J.H., J.A.D.), Kaiser Permanente Northern California, Oakland, California; Henry Ford Health Systems (C.N.-D.), Detroit, Michigan; HealthPartners Research Foundation (S.J.R., J.M.J.), Minneapolis, Minnesota; Center for Health Research, Northwest/Hawaii (M.C.H., D.J.B.), Kaiser Permanente Northwest, Portland, Oregon; and Division of Cancer Prevention and Control (S.S.C.), United States Centers for Disease Control and Prevention, Atlanta, Georgia, USA
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Open ArchivePublished:July 09, 2007DOI:https://doi.org/10.1016/j.jpainsymman.2006.11.011

      Abstract

      Women dying of ovarian cancer vary considerably in their complications and in the types of health care they receive. The objective of this study was to describe the complications of ovarian cancer, other than pain, and their treatment at the end of life. This study used a cohort of 421 enrollees in three nonprofit managed-care organizations who died with ovarian cancer during 1995–2000. Data were collected from abstraction of paper and electronic medical records. Proportions of women experiencing complications and undergoing treatments were calculated. Logistic regression was used to evaluate the association of patient characteristics with the probability of receiving an intervention for complications. The most common complications recorded in the medical record were fatigue or weakness (75%), nausea or vomiting (71%), constipation (49%), edema of the extremities (44%), and anemia (34%). The prevalence of major complications was as follows: ascites, 28%; bowel obstruction, 12%; pleural effusion, 10%; bladder obstruction, 3%; and disordered nutrition that required support with parenteral nutrition, 9%. Patients may not always have received interventions for major complications; for example, pleural effusion apparently was left untreated in almost half of the women with this problem. After adjustment, women who died at younger ages were more likely to receive an intervention, compared to older women (odds ratio for each decade of age, 0.71, 95% confidence interval=0.53, 0.94, P for trend=0.02). The study, which preceded the establishment of palliative care programs, suggests that care given to ovarian cancer patients at the end of life may be inadequate.

      Key Words

      Introduction

      Ovarian cancer is the leading cause of gynecologic cancer death among U.S. women. In 2005, perhaps 16,000 died from ovarian cancer. Most women are diagnosed at an advanced stage of the disease; five-year survival is 45%.
      Currently, there is a paucity of literature on end-of-life issues in ovarian cancer or, more generally, gynecologic cancers. The objective of this study was to estimate the occurrence of complications, and to describe treatment for those complications, during the last six months of life for women with ovarian cancer. We previously reported on the occurrence and management of pain in this population.
      • Rolnick S.J.
      • Jackson J.
      • Nelson W.
      • et al.
      Pain management in the last six months of life for women who died of ovarian cancer.
      Information about complications other than pain also could be of use to providers who are attempting to alleviate suffering, which is the ultimate goal when caring for patients dying of ovarian or any other cancer. By better understanding the treatment experiences of these women, physicians may identify opportunities to improve care. This information also might help patients and families anticipate specific symptoms, ease their fears of the unknown, and help them set realistic expectations. Moreover, information on the spectrum of palliative care that might be offered could help direct patients and their families to clinically appropriate interventions and allow them to participate in the discussion of options for palliative treatment both earlier on, and with greater acceptance.

      Methods

      Participants

      The study was conducted at three managed-care organizations that had integrated delivery systems and computerized cancer registries. We included all women aged 18 years and older who died of epithelial ovarian cancer during the six-year period 1995–2000. This study period precedes the establishment of palliative care programs at the health plans, with care having been provided primarily by the oncologist and hospital staff. At one plan, only women diagnosed in 1995 or later were included, whereas at the other two plans, women may have been diagnosed earlier than 1995. Enrollees who died from ovarian cancer were identified by matching enrollment databases at the health plans to data from cancer registries and information on deaths from vital statistics offices at the State level. Each case's cause of death was confirmed by abstracting the chart, and women whose primary cause of death was not ovarian cancer or a complication of that disease were excluded (n=13). In addition, women whose charts were missing or substantially empty were not included in the study (n=16). In all, 421 women were eligible for the study.

      Data Collection

      Two methods were used to collect data: a) linkage with electronic data, and b) manual review of medical records. Data pertinent to this report included the patient's demographic factors (age, race/ethnicity, marital status, location of residence); tumor characteristics; recurrences; information about signs and symptoms at the end of life, including interventions; and comorbid conditions. Most information was obtained for the last six months of life (or from diagnosis to death for women who died within six months of diagnosis).

      Linkage with Electronic Data

      Variables obtained from linkage included information on the diagnosis and the death, the concentration of cancer antigen 125 (CA-125), use of psychotropic drugs, and comorbidity. In general, data were extracted from computerized information systems for the six months before death; data on comorbidity were based on the period 18 months to six months before death. Information on CA-125 was obtained from computerized laboratory tests, whereas information on dispensing of psychotropic medications was obtained from outpatient pharmacy records.

      Review of Medical Records

      Variables obtained from review of the medical record included information on the patient's demographic and social characteristics; complications, recurrences, and medical procedures; and patient preferences for stopping curative care and accepting the end of life. Interventions were ascertained for five major complications: ascites, pleural effusion, bowel obstruction, bladder obstruction, and nutritional disorders. Where there was no record of treatment, we assumed that treatment had not been provided. Trained medical record analysts were provided with a standardized instrument and codebook for abstracting the chart. The codebook included question-by-question specifications and background materials as well as abstracting protocols. Direct input of data was achieved through a computerized data entry and management program developed using Microsoft Access® that included range and logic checks. To further ensure quality and consistency of the data across the three sites, we held biweekly conference calls involving all study personnel, including abstractors, to answer questions and review their productivity and the quality of work.

      Data Analysis

      We examined for specific time periods before death the proportion of women who experienced certain signs or symptoms, underwent various measurements, and received procedures of interest. Logistic regression was used to model the association of age at death, race or ethnicity, marital status, stage of disease, interval between diagnosis and death, and comorbidity with the probability of receiving an intervention for complications incurred during the last six months of life. Because the literature on palliative care does not consider declining appetite or thirst to be a reason for intervening with the dying patient, we did not treat nutrition-related complications as representing poor outcomes in this study. We could not consider interventions for fatigue/weakness, nausea/vomiting, constipation, edema of extremities, or anemia, as we did not obtain data on how these problems were treated.

      Results

      About 90% of women were aged 50 years or older at diagnosis and death (Table 1), all but 17% were white non-Hispanic, and 50% were married or living with a partner. Almost one-quarter of the women lived alone, 2% in a nursing home, and most of the remainder in a home with other people. Of those with unknown place of death, 51% were referred to hospice, 24% died in the hospital, 9% in a skilled nursing facility, and 36% in a private home. About three-quarters had been diagnosed initially with metastatic disease. The average CA-125 concentration during the last six months of life varied considerably. The interval between diagnosis and death was less than one month for 11% of patients, but three years or more for 14%. Just over half of the patients had no comorbid conditions, 33% had one or two, and 14% had three or more.
      Table 1Characteristics of the 421 Study Participants
      Characteristicsn%
      Age at diagnosis (y)
       <504811
       50–599022
       60–6911327
       70+17040
      Age at death (y)
       <50379
       50–598520
       60–6911227
       70+18744
      Race or ethnicity
       African American338
       Asian174
       White, non-Hispanic34883
       Hispanic184
       Native American<5<1
       Unknown41
      Needs interpreter
       Yes184
      Marital status
       Married20549
       Living together41
       Separated/divorced6616
       Widowed10826
       Single, never married327
       Unknown61
      Residence during the last six months of life
       Alone in own home9823
       Own home with dependent children215
       Own home with independent adult20749
       Friend's or relative's home4310
       Nursing home72
       Other4410
      Hospice referral21451
      Place of death
       Hospital10324
       Patient's home13733
       Relative's home143
       Skilled nursing facility369
       Hospice61
       Other82
       Unknown11728
      Diagnosis year
       <1995389
       1995–199617341
       1997–199814334
       1999–20006716
      Summary stage of disease
       Localized133
       Regional6916
       Distant metastases or systemic disease31074
       Not determined297
      Average CA-125 concentration during last six months (U/ml)
       No measurement7919
       5–1208520
       121–4108621
       411–15148520
       1,515 or more8620
      Interval between diagnosis and death
       <1 mo4511
       4–11 mo8119
       12–23 mo10826
       24–35 mo6215
       ≥3 y6014
      Number of comorbidities
       022253
       1–213933
       3–76014
      Note in chart that patient never accepted terminal conditions215
      Note in chart that patient asked for cessation of curative care348
      The most common complications recorded in the medical record during the last six months of life were fatigue or weakness (75%), nausea or vomiting (71%), constipation (49%), edema of the extremities (44%), and anemia (34%) (Table 2). Other than nutrition, the most common major complications were ascites (28%), bowel obstruction (12%), pleural effusion (10%), and bladder obstruction (3%). Disorders of nutrition were indicated in the medical record with a range of descriptors, from “loss of appetite” to intensive interventions such as parenteral nutrition (9%).
      Table 2Complication and Concomitant Intervention Occurrence in the Six Months Prior to Death
      Complication and Intervention
      A woman could have been counted with more than one kind of intervention for the same type of complication (e.g., two separate “episodes” or occurrences of bowel obstruction, each with a different intervention, e.g., no intervention and abdominal surgery).
      Time Period (From End of Life)
      0–6 mo0–60 d0–30 d0–14 d
      % of Cohort (n=421)
      Ascites
      Overall proportion with any episode of this kind of complication that occurred during the specified time period.
      27.517.110.94.0
       No intervention18.510.75.72.4
       Tumor debulking1.70.70.70.2
       Paracentesis8.56.24.51.2
       Other intervention1.71.20.50.2
      Pleural effusion
      Overall proportion with any episode of this kind of complication that occurred during the specified time period.
      10.07.14.02.1
       No intervention4.52.61.40.9
       Tumor debulking0.50.50.50.2
       Thoracentesis4.73.31.90.9
       Other intervention
      A woman could have been counted with more than one kind of intervention for the same type of complication (e.g., two separate “episodes” or occurrences of bowel obstruction, each with a different intervention, e.g., no intervention and abdominal surgery).
      1.40.70.20
      Bowel obstruction
      Overall proportion with any episode of this kind of complication that occurred during the specified time period.
      11.66.44.51.7
       No intervention4.32.62.10.9
       Abdominal surgery6.63.11.90.5
       Palliative chemotherapy0.20.200
       Palliative radiation0.20.20.20.2
       Other intervention0.70.20.20
      Bladder obstruction
      Overall proportion with any episode of this kind of complication that occurred during the specified time period.
      2.81.91.40.5
       No intervention0.90.50.50.5
       Abdominal surgery
      Overall proportion with any episode of this kind of complication that occurred during the specified time period.
      1.41.20.70
       Other intervention0.90.70.20
      One or more of the complications listed above
       No61.174.482.492.6
       Any complication, but without intervention18.111.48.14.0
       Any complication, with at least one intervention20.914.39.53.3
      Nutrition interventions
      Mutually exclusive categories based on hierarchical assignment of nutritional intervention (parenteral nutrition support>tube feedings>dietitian consult>dietary supplements).
       Dietary supplements
      Oral liquid supplements primarily (e.g., Ensure®, Instant Breakfast®).
      11.45.93.31.2
       Dietitian consult1.21.20.90.7
       Tube feedings
      Nasogastric, gastrostomy, jejunostomy tube feedings.
      1.91.91.70.7
       Parenteral nutrition support
      Includes intravenous hydration and total parenteral nutrition.
      9.35.22.61.4
      Timing of last tumor recurrence (n=154)36.011.05.02.0
      Psychotropic medication use
       Antidepressants only7.17.39.510.0
       Antianxiety drugs34.931.829.727.8
       Both22.318.815.211.6
       Neither32.138.542.047.0
       No use of outpatient pharmacy3.63.63.63.6
      Selected other symptoms
      Overall proportion with any episode of this kind of complication that occurred during the specified time period.
      97.459.635.919.0
       Fatigue/weakness74.623.011.45.2
       Nausea/vomiting70.826.411.95.7
       Constipation48.519.99.74.3
       Edema of extremities44.418.811.95.7
       Anemia33.712.35.23.3
      a A woman could have been counted with more than one kind of intervention for the same type of complication (e.g., two separate “episodes” or occurrences of bowel obstruction, each with a different intervention, e.g., no intervention and abdominal surgery).
      b Overall proportion with any episode of this kind of complication that occurred during the specified time period.
      c Mutually exclusive categories based on hierarchical assignment of nutritional intervention (parenteral nutrition support>tube feedings>dietitian consult>dietary supplements).
      d Oral liquid supplements primarily (e.g., Ensure®, Instant Breakfast®).
      e Nasogastric, gastrostomy, jejunostomy tube feedings.
      f Includes intravenous hydration and total parenteral nutrition.
      About two-thirds of women with ascites were not treated for the condition. Pleural effusion was treated in about half of the women with this problem. For bowel or bladder obstruction, there was no treatment in about one-third of affected women. Four women had abdominal surgery to treat effusion or a bowel obstruction during the last 14 days of life. Thirty-six percent of women had a tumor recurrence during the last six months of life. Thirty-five percent of women received antianxiety medications during the last six months; only 7% used antidepressants during that time, but that number rose to 10% for the final 14 days.
      Nutrition-related interventions declined noticeably with the approach to death (Table 2). Dietary supplements were given fairly often to women who experienced a nutritional problem in the final six months of life, but they were infrequently supplied in the final 14 days (1.2%). Parenteral nutrition support was somewhat less common than dietary supplements during the final six months, and in the final 14 days, very few women received this intervention (1.4%). Tube feedings were infrequent (less than 2% through the final six-month period).
      Differences were observed by age at death for the probability of receiving an intervention for pleural effusion, ascites, or obstruction of the bowel or bladder. After adjustment for marital status, race or ethnicity, comorbidity, and the interval between diagnosis and death, women who died at younger ages were more likely than older women to receive an intervention (data not shown), with the odds ratio for each decade of age equaling 0.71 (95% confidence interval=0.53, 0.94, P for trend=0.02). No differences were found in the likelihood of intervention by race or ethnicity, marital status, stage of disease, interval between diagnosis and death, or comorbidity.

      Discussion

      In this investigation of women who died of ovarian cancer, we observed that for some complications that might lead to a relatively difficult death, there was no record of treatment, and we concluded that treatment was not offered. Failure to offer treatment was seen frequently for women with pleural effusion, ascites, and obstruction of the bowel or bladder. In addition, numerous women with many months of life remaining were not offered treatment for a major complication. In the case of pleural effusion, we found no record of intervention for 45% of the women who suffered this problem in the last six months of life. The treatment for pleural effusion, thoracentesis, poses a slight risk for infection and damage to the lung itself, but the dyspnea and chest pain that result from this complication can frighten patients and their caregivers. Because the ultimate goal of palliative care is to maximize the patient's comfort, the relief that treatment could provide may well compensate for the risk of the procedure.
      Obstruction of the bowel and bladder are most often treated with abdominal surgery. The potential benefit in life expectancy from surgery can be as long as several months. However, this must be weighed against the operative risks, especially among women with poor health status.
      We observed a sharp increase in compromised nutrition, together with a sharp decline in management, during the last two weeks of life. Early on in the dying process, maintenance of nutrition may be used to achieve specific ends, such as to give the woman enough stamina to participate in a special event. When death becomes very close, there may not be hunger, and maintaining nutrition may no longer be relevant. In addition, feeding tubes and parenteral nutrition add to the risk of infection, may be poorly tolerated in these patients, and may cause cramps and diarrhea, thereby reducing quality of life.
      The literature on palliative care is clear that hydration, per se, is not a goal of treatment in the dying patient.
      • De Ridder D.
      • Gastmans C.
      Dehydration among terminally ill patients: an integrated ethical and practical approach for caregivers.
      • Zerwekh J.V.
      Do dying patients really need IV fluids?.
      • Taylor M.A.
      Benefits of dehydration in terminally ill patients: allowing terminally ill patients to dehydrate is an ethically and legally acceptable therapeutic measure.
      Indeed, it has been proposed that dehydration in dying patients has some therapeutic value (e.g., reduced incontinence, less nausea and vomiting, and fewer pulmonary secretions) and may even produce some analgesic effects. Furthermore, interventions for compromised nutrition, such as the placement of feeding tubes and implementation of parenteral nutrition, pose risks for infection.
      Two limitations of our study should be borne in mind. First, a retrospective examination of the final six months of life involves a different perspective from that of the physicians and other professionals who cared for the women in this study. In the actual care environment, for example, the perceived terminal phase could have started well before the final six months for some women, and treatment for some of the problems we examined may have actually been given prior to our study period (while we classified it as not given because it was not in the final six months). The actual effect of these limitations on our results would probably have been modest, however.
      The second limitation concerns the use of medical record data for ascertaining complications and their treatment. Use of medical records for ascertaining symptoms among dying patients was examined in a study by Stromgren et al.
      • Stromgren A.S.
      • Groenvold M.
      • Pedersen L.
      • et al.
      Does the medical record cover the symptoms experienced by cancer patients receiving palliative care? A comparison of the record and patient self-rating.
      of Danish patients with advanced cancer. These investigators assessed the concordance of the medical record with patients' self-reported symptoms and found the medical record to provide lower estimates of symptoms than those provided by patient reports: fatigue (only 38% of patients' reports were noted in the medical record), nausea/vomiting (52%), constipation (38%), depression (25%), anxiety (20%), and reduced appetite (51%). Their study included a range of cancer patients, but they did not report on the major complications of interest in the present study (ascites, pleural effusion, obstruction of bowel or bladder, and cachexia). Similarly, use of oxygen for dyspnea and other comfort measures could not be reliably obtained.
      Our findings are broadly consistent with a prospective study of symptoms among 1,000 patients with any type of cancer admitted to the Palliative Medicine Program of the Cleveland Clinic.
      • Walsh D.
      • Donnelly S.
      • Rybicki L.
      The symptoms of advanced cancer: relationship to age, gender, and performance status in 1,000 patients.
      The most prevalent symptoms observed, other than pain, were fatigue, weakness, anorexia, lack of energy, dry mouth, constipation, early satiety, dyspnea, and weight loss, with these symptoms occurring in 50%–84% of patients. One challenge with comparing results across studies is the imprecise definition of these symptoms and lack of standardized assessment. Standardized assessments have been tested in Germany, with large variation in documentation among palliative care units across the country.
      • Radbruch L.
      • Nauck F.
      • Fuchs M.
      • et al.
      What is palliative care in Germany? Results from a representative survey.
      These authors recommend, and we concur, that standardized instruments are the first step toward furthering palliative care research, with training to standardize definitions following close behind.
      Another consideration may affect the generalizability of the study: it was set in three managed-care settings where patients have comprehensive health insurance coverage and do not face the overwhelming financial barriers to access that challenge uninsured patients. Hence, the observed variations in patterns of care for women with terminal ovarian cancer are more likely to be associated with the preferences of the patient, family, or provider, and with the managed-care structure of the delivery system.
      Besides seeking to identify opportunities to improve palliative care for women dying of ovarian cancer, we hoped to provide information that might be shared with patients and families with which to create expectations about their health status during the final months of life. In a study by Doyle et al.,
      • Doyle C.
      • Crump M.
      • Pintilie M.
      • Oza A.M.
      Does palliative chemotherapy palliate? Evaluation of expectations, outcomes, and costs in women receiving chemotherapy for advanced ovarian cancer.
      42% (n=27) of women with ovarian cancer who received palliative chemotherapy thought the treatment would have a moderate-to-high chance of curing their disease. This raises concerns that women with ovarian cancer misunderstand the objectives of end-of-life care and that they have unrealistic expectations about their chances for cure, which may lead them to demand aggressive care that reduces the quality of their life before death. An example would be abdominal surgery, although we observed only a small number (n=4) of abdominal surgeries undertaken during the last 14 days of life and cannot comment on their appropriateness.
      Since this study was begun, numerous palliative care programs have been established. We recommend evaluation of those programs using prospective study designs with systematic assessment of patient-reported pain and physical and psychological functioning. The perspectives of patients and caregivers and the role of functional status and cultural differences should be evaluated as well.

      Acknowledgments

      The authors wish to thank Richard L. Heinrich, MD for helpful review comments.

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