Defining Cancer Patients As Being in the Terminal Phase: Who Receives a Formal Diagnosis, and What Are the Effects?
http://www.100md.com
《临床肿瘤学》
the Research Units of General Practice, Health Economics, and Epidemiology, Institute of Public Health, University of Southern Denmark, Odense, Denmark
ABSTRACT
PURPOSE: Physicians either do not define cancer patients as being terminal, or their prognostic estimates tend to be optimistic. This might affect patients' appropriate and timely referral to specialist palliative care services or can lead to unintended acute hospitalization.
PATIENTS AND METHODS: We used the Danish Cancer Register and four administrative registers to perform a retrospective cohort study in 3,445 patients who died as a result of cancer. We used the Danish "terminal declaration" issued by a physician as a proxy for a formal terminal diagnosis (prognosis of death within 6 months). The terminal declaration gives right to economic benefits and increased care for the dying. We investigated patient-related factors of receiving an explicit terminal diagnosis by logistic regression and then analyzed the effects of such a diagnosis on admission rate per week and place of death.
RESULTS: Thirty-four percent of patients received a formal terminal diagnosis. Age of 70 years (odds ratio [OR], 0.44; 95% CI, 0.34 to 0.56; P < .001), women (OR, 0.81; 95% CI, 0.69 to 0.96; P = .02), hematologic cancer (OR, 0.20; 95% CI, 0.09 to 0.41; P < .001), and a less than 1-month survival time (OR, 0.10; 95% CI, 0.07 to 0.15; P < .001) were associated with a lesser likelihood of receiving a formal terminal diagnosis. Explicit terminal diagnosis was associated with lower admission rate and an adjusted OR of hospital death of 0.25 (95% CI, 0.21 to 0.29).
CONCLUSION: Women and the elderly were less likely to receive a formal terminal diagnosis. The formal terminal diagnosis reduced hospital admissions and increased the possibilities of dying at home.
INTRODUCTION
Deciding that a cancer course has come to a terminal phase is an ongoing challenge for physicians.1-3 Despite development of prognostic models and instruments for predicting survival in patients with late-stage cancer who are hospitalized,4,5 most physicians either do not define patients as being terminal or their prognostic estimates tend to be optimistic,6-8 particularly with regard to those patients who die soon after the cancer diagnosis.9 This might affect patients' appropriate and timely referral to specialist palliative care services10 or can lead to unplanned hospitalization because of poorly coordinated or otherwise inadequate supportive care services being available at home.11 It also may lead to problems, such as poor symptom control (ie, restricted morphine prescription)12-14 or "carer fatigue" caused by insufficient support to the informal carer.15,16 Defining a patient as terminal might provide opportunities to plan the terminal phase17 that, in the end, could result in a better-quality end of life for the patient and his or her carer.18
Entering the terminal phase of a cancer disease may be clinically recognized by indistinct patterns, such as lack of response to treatment, increased disease progression, the onset of anorexia, or the loss of will to live. Cancer type may be of importance for terminal definition, because some types have a well-known poor prognosis (eg, lung19 and pancreatic20 cancers). This might facilitate definition of the terminal status, whereas other types of cancers or an inaccurate diagnosis might tend to hold back a clear terminal diagnosis. In the elderly a cancer disease might be less obvious or less well-diagnosed because of comorbidity. This could hamper or delay a clear terminal diagnosis.
Because of a special reimbursement system in Denmark, we are able to use a proxy for entrance into the terminal phase of a cancer disease: the "terminal declaration" (TD). Before signing a TD, the responsible physician has to actively define the patient as having a terminal illness with a prognosis of death within 6 months. The signed formula gives patients the right to increased reimbursement for medicine and an informal carer to be entitled to full-time or part-time paid leave. The TD is therefore an explicit terminal diagnosis issued by the patient's general practitioner, oncologist, or other specialist. Implicit or latent terminal diagnoses exist: situations in which a TD is not signed, although the physician, the patient, or the family involved has a sense of an approaching death. Our hypothesis, however, is that an explicit and observed terminal diagnosis has beneficial consequences for end-of-life care (ie, will avoid lengthy hospital admissions or death in acute care settings).21-24
The aim of this study was to find population-based patient-related factors of importance for the explicit terminal diagnosis and to analyze the implications of such a diagnosis on some important and measurable parameters of the quality of end-of-life care in cancer.
PATIENTS AND METHODS
the Danish Civil Registration System,25 we identified all persons who died in the County of Funen in the period 1996 to 1998 (Fig 1). The study population was identified by linkage to the files of the Danish Cancer Registry.26,27 Since 1943 the registry has collected information on all individuals in Denmark with cancer. The registration is based on notification forms that are completed by hospital departments and general practitioners whenever a case of cancer is diagnosed or found at autopsy and whenever there are changes to an initial diagnosis. By annual linkages to the death certificate files the cause of death is noted. Ambiguous or contradictory information, either within a notification form or between forms, leads to queries in approximately 10% of the notifications received. Comprehensive evaluation has shown that the registry is 95% to 99% complete and valid.28-30
The study population of patients with cancer as the primary cause of death was linked with the Danish Hospital Discharge Register, which has kept records of nearly all (99%) the somatic hospitalizations in Denmark since 1977.31 The register receives new data from all Danish hospitals once a month. This computerized central register contains, for each discharge, information on the personal identification number of the patient; dates of admission and discharge, up to 20 diagnoses; and every surgical procedure performed during the respective admission besides all outpatient contacts by date and diagnosis. Ad hoc validation of the administrative information has shown agreement in 98.5% of the cases. Finally, the study population was linked with registration of the TD in the municipalities. The unique identification number assigned to everyone living in Denmark ensured accurate, individual-based linkage of information between registers.
Primary cause of death was categorized into six categories: four separate categories for the four most frequent cancers (lung, breast, colon-rectum, and prostate), one category for the hematologic cancers (the course of which is rapid and treatment for which is intense), and one final category containing other cancers. Age was categorized as 18 to 29, 30 to 39, 40 to 49, 50 to 59, 60 to 69, 70 to 79, and 80 years. Finally, being married and having children were dichotomized.
In Denmark most health care costs are tax funded. All hospital care and most primary care are free of charge for the patients. Expenses for drugs, however, are only partly subsidized. In the study period, a TD could be issued to patients by a physician (general practitioner or hospital physician) if the physician found the patient to be terminal (not likely to benefit from curable treatment and not likely to live for > 6 months). Informed consent from the patient was needed. The TD entitled the patient to full reimbursement for drug expenses, reimbursement of expenses for equipment used in home care, and payment to informal caregivers. The TD has existed since 1990 and is well known by physicians, patients, and relatives.
Individual follow-up began 90 days before death or at the date of diagnosis (if it was less than 90 days before death) and ended at the date of death. For the TD, however, we could also collect the exact date of registration before the 90 days of follow-up. We first used the TD as a binary outcome variable and hence estimated the odds ratio (OR) of TD by logistic-regression models and calculated 95% CIs. In the models we adjusted for potential confounding factors. Age could be a confounder because elderly people may delay seeking medical advice for suspicion of cancer, and analogous to this we assume they may also delay seeking help in a terminal phase. Sex also must be considered a confounder because of different health service utilization by men and women, and type of cancer because different types of cancer have distinctly different natural courses of disease. Being married and having children are also possible confounders, because informal carers are able to ask for assistance and support in the health care system. As expected, we found a dependency between the odds of TD and week number before death, which we allowed for by including a separate constant for each week on which the risk of TD could depend. In the second analysis, we estimated the rate of admission to hospital for patients with a cancer diagnosis (a maximum of 12 weeks, accounting only for the time period after the diagnosis of cancer) by using TD as a binary covariate. Finally, we analyzed the risk of hospital death by logistic regression. All analyses were conducted by using STATA 8 (STATA Corp, College Station, TX).
RESULTS
For 34% of the patients in the total cohort (n = 3,445), the physician signed a TD (Fig 1). However, when survival time (ie, time from cancer diagnosis until death) was less than 1 month, only 8% received a TD. The declaration was signed a median of 52 days (interquartile range, 20 to 105) before death, with a mean of 100 days (95% CI, 91 to 110) (Table 1).
We found the probability of a TD to be significantly lower in the 70-year age groups and after eliminating patients living in a nursing home (n = 225). Female sex compared to male sex and hematologic cancers compared to "other" cancers showed significantly lower probability of a TD, whereas being married versus being single (widowed, divorced, or not married) and having cancer of the prostate or lung increased the probability of a TD (Table 2). Looking at the patients (n = 619) with short survival time ( 1 month), we found the same age distribution as in the total cohort. However, we found significantly fewer cancers with a known extended course (ie, prostate and breast cancers).
Looking at the effects of TD, we found that the admission rate increased less with TD (Fig 2). Interestingly, however, we found significantly longer admission time with TD (35.3 v 30.2 days). In our cohort, 56% (n = 1,935) died in the hospital, 28% (n = 965) died at home, 16% (n = 518) died in a nursing home, and 1% had an unknown place of death. Hospital death was found in 65% (n = 1,487) of cancer patients without TD, whereas only 39% (n = 448) of cancer patients with a TD died in the hospital. With a TD, the adjusted OR of hospital death was 0.25 (95% CI, 0.21 to 0.29).
DISCUSSION
A TD was signed for one third of terminal cancer patients. Significantly fewer elderly ( 70 years) and female patients were observed to receive a TD. An explicit terminal diagnosis seemed to reduce admission rates and reduced the risk of dying in an acute care setting.
This study has the strength of being a large population-based study in which the effect of selection bias is minimized because of the design of the cohort, which consists of all deceased cancer patients in a clearly defined time interval and a well-defined geographical area. The data collection was based on the complete population-based registries in Denmark, comprising uniform and identifiable information on deaths, hospitalizations, cancer development, and vital status. The personal identification number from the Danish Civil Registration Register ensures reliable record linkages of information. The validity of the Danish Cancer Register is high compared with other disease registers, and the National Discharge Register concerning the administrative data has been validated, showing an agreement of 98.5%.
However, there are some limitations to this study that deserve consideration. First, misclassification might have occurred by using the written declaration as a proxy for the terminal diagnosis. Because the TD carries with it benefits for reimbursement for expenses (medicine and equipment for home care), especially paid leave for informal caregivers, it may reflect more than simply the prognosis of the patients. For example, caregivers for the elderly (who may be old-age pensioners themselves) are less likely to benefit from paid leave from work. Although the declaration would have other advantages for such patients (and patients without a caregiver), they might be less likely to receive a TD. The TD, therefore, is most reliable as a proxy for a terminal diagnosis in patients with a positive TD. For patients without a TD, we cannot be sure that the physician did not make up his or her mind (diagnosing the patient as terminal). The physician may have made an implicit diagnosis. The administrative work of signing the declaration or patients considered without need of financial support might have held back the physician from signing a TD. In addition, the physician might weigh the advantages against the disadvantages of confronting the patient and the family with a terminal diagnosis. Studies have shed light on the existence of this bias. Collusion in doctor-patient communication has acted as a mechanism of delayed TD,32 and family physicians have been less willing to diagnose patients as terminal compared with other doctors.33 From the patient's point of view, patient coping strategies constrained an information-seeking behavior.34 Especially patients, but also informal carers, wish to maintain hope.35 Professionals, therefore, may have treated some of the patients without a TD as terminal patients. This type of misclassification may lead to some degree of underestimation of the effects of the terminal diagnosis. In another scenario, if the patient showed no sign of an approaching death, we could not expect the physician to sign a TD.36 However, when analyzing patient characteristics for receiving a terminal diagnosis, we analyzed at the point of death, at which we assume there ought to be signs of approaching death. In our analysis of the effects of terminal diagnosis, we broke down the total follow-up period into shorter intervals of time (weeks) and by this demonstrated an increasing effect as death approaches.
Not all patients dying from cancer will have the possibility of receiving a TD. Patients who died as the result of a potentially curative therapy, such as surgery or adjuvant or aggressive first-line chemotherapy, will probably not have been considered terminal. Those patients will probably die in an acute care setting, which in this study may overestimate the effect of terminal diagnosis. Such patients, however, are likely to be relatively few. The signed TD was collected from each municipal administration. Because of incomplete or missing information, we had to eliminate 13 small municipalities with a total of 941 cancer patients. However, those 941 patients were comparable to the rest of the cohort with regard to age, sex, marital status, children, and types of cancer. Finally, existence of some degree of misclassification in the registration system in the municipal administration must be considered. Misclassification caused by incomplete or erroneous registration in the municipal administration, however, is likely to be nondifferential with respect to the studied variables and in any case will tend to be reduced by the routinely conducted external auditing.
The risk of admission was initially higher among patients with a terminal diagnosis in the beginning of the 90-day period. We interpret this as being because of increased severity of the disease (ie, the more severe the illness the easier to detect a patient as terminal). If this interpretation is accurate, our results are even more important: Despite a more severe disease, patients with TD had fewer hospital admissions and more often died at home. The overall rate of hospital death in our study was similar to figures previously published for the US (56% v 52%).37
To our knowledge, only few population-based studies have analyzed patient-related factors associated with the physician decision about a terminal diagnosis. Hospice referral often implies more intensive treatment, and in North America the average patient stays less than 3 weeks in a hospice before dying.38 A diagnosis of "terminal stage" can often be made earlier, and the median period of survival after receiving a TD in our study was more than double (52 days). Many patients are not in need of intensive terminal care when they receive the TD. It is important to emphasize that a TD does not change the patient's overall rights in the Danish health care system; for example, the patient does not relinquish any acute care benefits as a consequence. In contrast, referral to a hospice may change the health care access for patient and family in the US Medicare program, which may have an influence on the timing of hospice entrance.39
In our study we found that fewer female and fewer elderly cancer patients received a terminal diagnosis even after adjusting for important confounders. The sex difference could be explained by the fact that women are still the primary caregivers in the family and hence are more proactive in getting the services needed for their spouse. That elderly patients are less likely to get a TD can be explained partially by the fact that elderly cancer patients are more reluctant to contact health care services, which can be seen by the relationship between increasing age and advanced stage of the disease at the time of diagnosis.40 From a health care service point of view, elderly patients ( 65 years) were less likely to receive cancer-related treatment,41 and physicians tend to undertreat pain in older patients.42 The elderly were also found to suffer delays in accessing terminal benefits,43 which correspond well with our results. As expected, short survival time (ie, time from cancer diagnosis until death) was found to reduce the proportion receiving a TD. Aggressive progression of the disease provides a reduced amount of time for the physician to detect a beginning terminal phase.
Our results, based on administrative databases, cannot elucidate mechanisms in doctor-patient communication or mechanisms in patient or doctor inner life. However, the use of administrative data can provide a practical and economical tool for profiling quality of care or screening for problems with care. For the health care providers, our studies show the importance of making the terminal diagnosis explicit. It is not surprising that an explicit terminal diagnosis facilitates planning of palliative care and thus has an effect on end-of-life care. Only 34% of the patients in our study received a TD. The late recognition of an approaching death might not allow healthcare professionals to discuss the feasibility of care and death at home. What is more important is that our results shed additional light on the probably insufficient services for some subgroups of end-stage cancer patients. Additional studies should focus on those groups to facilitate the necessary access to palliative care services.
Authors' Disclosures of Potential Conflicts of Interest
The authors indicated no potential conflicts of interest.
Acknowledgment
We thank G. Engholm and H.H. Storm from the Department of Cancer Prevention and Documentation, Danish Cancer Society, for inspiring input into the planning phase and access to data from the Danish Cancer Register. We also thank P. Pedersen from the Municipality of Odense for access to data from the Department for the Elderly and Disabled in Odense.
NOTES
Supported by the Health Insurance Foundation (Grants No. 2001B116 and 2002B025), the Danish Research Foundation for General Practice (Grant No. 586-193259), and the Danish College of General Practitioners' Foundation for Research in General Practice 2001.
Authors' disclosures of potential conflicts of interest are found at the end of this article.
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Gordon EJ, Daugherty CK: Hitting you over the head: Oncologists' disclosure of prognosis to advanced cancer patients. Bioethics 17:142-168, 2003
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Glare P, Virik K, Jones M, et al: A systematic review of physicians' survival predictions in terminally ill cancer patients. BMJ 327:195, 2003
Christakis NA, Lamont EB: Extent and determinants of error in doctors' prognoses in terminally ill patients: Prospective cohort study. BMJ 320:469-472, 2004
Chow E, Harth T, Hruby G, et al: How accurate are physicians' clinical predictions of survival and the available prognostic tools in estimating survival times in terminally ill cancer patients? A systematic review. Clin Oncol (R Coll Radiol) 13:209-218, 2001
Vigano A, Dorgan M, Bruera E, et al: The relative accuracy of the clinical estimation of the duration of life for patients with end of life cancer. Cancer 86:170-176, 1999
Brinckner L, Scannell K, Marquet S, et al: Barriers to hospice care and referrals: Survey of physicians' knowledge, attitudes, and perceptions in a health maintenance organization. J Palliat Med 7:411-418, 2004
Abom B, Obling N, Rasmussen H, et al: Unplanned emergency admission of dying patients: Causes elucidated by focus group interviews with general practitioners. Ugeskr Laeger 162:5768-5771, 2000 [in Danish]
Zenz M, Willweber-Strumpf A: Opiophobia and cancer pain in Europe. Lancet 341:1075-1076, 1993
Bercovitch M, Adunsky A. Patterns of high-dose morphine use in a home-care hospice service: Should we be afraid of it? Cancer 101:1473-1477, 2004
Carr DB, Goudas LC, Balk EM, et al: Evidence report on the treatment of pain in cancer patients. J Natl Cancer Inst Monogr 32:23-31, 2004
Grunfeld E, Coyle D, Whelan T, et al: Family caregiver burden: Results of a longitudinal study of breast cancer patients and their principal caregivers. CMAJ 170:1795-1801,2004
Visser G, Klinkenberg M, Broese van Groenou MI, et al: The end of life: Informal care for dying older people and its relationship to place of death. Palliat Med 18:468-477,2004
Saunders Y, Ross JR, Riley J. Planning for a good death: Responding to unexpected events. BMJ 327:204-207,2004
Steinhauser KE, Christakis NA, Clipp EC, et al: Factors considered important at the end of life by patients, family, physicians, and other care providers. JAMA 284:2476-2482, 2000
Earle CC: Outcomes research in lung cancer. J Natl Cancer Inst Monogr 33:56-77, 2004
de Braud F, Cascinu S, Gatta G. Cancer of pancreas. Crit Rev Oncol Hematol 50:147-155, 2004
Earle CC, Park ER, Lai B, et al: Identifying potential indicators of the quality of end-of-life cancer care from administrative data. J Clin Oncol 21:1133-1138, 2003
Townsend J, Frank AO, Fermont D, et al: Terminal cancer care and patients preference for place of death: A prospective study. BMJ 301:415-417, 1990
Tiernan E, O'Connor M, O'Siorain L, et al: A prospective study of preferred versus actual place of death among patients referred to a palliative care home-care service. Ir Med J 95:232-235, 2002
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Storm HH, Michelsen EV, Clemmensen I, et al: The Danish Cancer Registry: History, content, quality and use. Dan Med Bull 44:535-539, 1997
Storm HH: Health care system, cancer registration and follow-up of cancer patients in Denmark. IARC Sci Publ 132:48-50, 1995
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The AM, Hak T, Koeter G, et al: Collusion in doctor-patient communication about imminent death: An ethnographic study. BMJ 321:1376-1381, 2000
Farquhar M, Grande G, Todd C, et al: Defining patients as palliative: Hospital doctors' versus general practitioners' perceptions. Palliat Med 16:247-250, 2002
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de Haes H, Koedoot N. Patient centered decision making in palliative cancer treatment: A world of paradoxes. Patient Educ Couns 50:43-49, 2003
Bach P, Schrag D, Begg CB: Resurrecting treatment histories of dead patients. JAMA 292:2765-2770, 2004
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McCarthy EP, Burns RB, Ngo-Metzger Q, et al: Hospice use among Medicare managed care and fee-for-service patients dying with cancer. JAMA 289:2238-2245, 2003
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Earle CC, Neville BA, Landrum MB, et al: Trends in the aggressiveness of cancer care near the end of life. J Clin Oncol 22:315-321, 2004
Bernabei R, Gambassi G, Lapane K, et al: Management of pain in elderly patients with cancer. SAGE Study Group: Systematic Assessment of Geriatric Drug Use via Epidemiology. JAMA 279:1877-1882, 1998
Nosowska G: A delay they can ill afford: Delays in obtaining attendance allowance for older, terminally ill cancer patients, and the role of health and social care professionals in reducing them. Health Soc Care Community 12:283-287, 2004(B. Aabom, J. Kragstrup, H)
ABSTRACT
PURPOSE: Physicians either do not define cancer patients as being terminal, or their prognostic estimates tend to be optimistic. This might affect patients' appropriate and timely referral to specialist palliative care services or can lead to unintended acute hospitalization.
PATIENTS AND METHODS: We used the Danish Cancer Register and four administrative registers to perform a retrospective cohort study in 3,445 patients who died as a result of cancer. We used the Danish "terminal declaration" issued by a physician as a proxy for a formal terminal diagnosis (prognosis of death within 6 months). The terminal declaration gives right to economic benefits and increased care for the dying. We investigated patient-related factors of receiving an explicit terminal diagnosis by logistic regression and then analyzed the effects of such a diagnosis on admission rate per week and place of death.
RESULTS: Thirty-four percent of patients received a formal terminal diagnosis. Age of 70 years (odds ratio [OR], 0.44; 95% CI, 0.34 to 0.56; P < .001), women (OR, 0.81; 95% CI, 0.69 to 0.96; P = .02), hematologic cancer (OR, 0.20; 95% CI, 0.09 to 0.41; P < .001), and a less than 1-month survival time (OR, 0.10; 95% CI, 0.07 to 0.15; P < .001) were associated with a lesser likelihood of receiving a formal terminal diagnosis. Explicit terminal diagnosis was associated with lower admission rate and an adjusted OR of hospital death of 0.25 (95% CI, 0.21 to 0.29).
CONCLUSION: Women and the elderly were less likely to receive a formal terminal diagnosis. The formal terminal diagnosis reduced hospital admissions and increased the possibilities of dying at home.
INTRODUCTION
Deciding that a cancer course has come to a terminal phase is an ongoing challenge for physicians.1-3 Despite development of prognostic models and instruments for predicting survival in patients with late-stage cancer who are hospitalized,4,5 most physicians either do not define patients as being terminal or their prognostic estimates tend to be optimistic,6-8 particularly with regard to those patients who die soon after the cancer diagnosis.9 This might affect patients' appropriate and timely referral to specialist palliative care services10 or can lead to unplanned hospitalization because of poorly coordinated or otherwise inadequate supportive care services being available at home.11 It also may lead to problems, such as poor symptom control (ie, restricted morphine prescription)12-14 or "carer fatigue" caused by insufficient support to the informal carer.15,16 Defining a patient as terminal might provide opportunities to plan the terminal phase17 that, in the end, could result in a better-quality end of life for the patient and his or her carer.18
Entering the terminal phase of a cancer disease may be clinically recognized by indistinct patterns, such as lack of response to treatment, increased disease progression, the onset of anorexia, or the loss of will to live. Cancer type may be of importance for terminal definition, because some types have a well-known poor prognosis (eg, lung19 and pancreatic20 cancers). This might facilitate definition of the terminal status, whereas other types of cancers or an inaccurate diagnosis might tend to hold back a clear terminal diagnosis. In the elderly a cancer disease might be less obvious or less well-diagnosed because of comorbidity. This could hamper or delay a clear terminal diagnosis.
Because of a special reimbursement system in Denmark, we are able to use a proxy for entrance into the terminal phase of a cancer disease: the "terminal declaration" (TD). Before signing a TD, the responsible physician has to actively define the patient as having a terminal illness with a prognosis of death within 6 months. The signed formula gives patients the right to increased reimbursement for medicine and an informal carer to be entitled to full-time or part-time paid leave. The TD is therefore an explicit terminal diagnosis issued by the patient's general practitioner, oncologist, or other specialist. Implicit or latent terminal diagnoses exist: situations in which a TD is not signed, although the physician, the patient, or the family involved has a sense of an approaching death. Our hypothesis, however, is that an explicit and observed terminal diagnosis has beneficial consequences for end-of-life care (ie, will avoid lengthy hospital admissions or death in acute care settings).21-24
The aim of this study was to find population-based patient-related factors of importance for the explicit terminal diagnosis and to analyze the implications of such a diagnosis on some important and measurable parameters of the quality of end-of-life care in cancer.
PATIENTS AND METHODS
the Danish Civil Registration System,25 we identified all persons who died in the County of Funen in the period 1996 to 1998 (Fig 1). The study population was identified by linkage to the files of the Danish Cancer Registry.26,27 Since 1943 the registry has collected information on all individuals in Denmark with cancer. The registration is based on notification forms that are completed by hospital departments and general practitioners whenever a case of cancer is diagnosed or found at autopsy and whenever there are changes to an initial diagnosis. By annual linkages to the death certificate files the cause of death is noted. Ambiguous or contradictory information, either within a notification form or between forms, leads to queries in approximately 10% of the notifications received. Comprehensive evaluation has shown that the registry is 95% to 99% complete and valid.28-30
The study population of patients with cancer as the primary cause of death was linked with the Danish Hospital Discharge Register, which has kept records of nearly all (99%) the somatic hospitalizations in Denmark since 1977.31 The register receives new data from all Danish hospitals once a month. This computerized central register contains, for each discharge, information on the personal identification number of the patient; dates of admission and discharge, up to 20 diagnoses; and every surgical procedure performed during the respective admission besides all outpatient contacts by date and diagnosis. Ad hoc validation of the administrative information has shown agreement in 98.5% of the cases. Finally, the study population was linked with registration of the TD in the municipalities. The unique identification number assigned to everyone living in Denmark ensured accurate, individual-based linkage of information between registers.
Primary cause of death was categorized into six categories: four separate categories for the four most frequent cancers (lung, breast, colon-rectum, and prostate), one category for the hematologic cancers (the course of which is rapid and treatment for which is intense), and one final category containing other cancers. Age was categorized as 18 to 29, 30 to 39, 40 to 49, 50 to 59, 60 to 69, 70 to 79, and 80 years. Finally, being married and having children were dichotomized.
In Denmark most health care costs are tax funded. All hospital care and most primary care are free of charge for the patients. Expenses for drugs, however, are only partly subsidized. In the study period, a TD could be issued to patients by a physician (general practitioner or hospital physician) if the physician found the patient to be terminal (not likely to benefit from curable treatment and not likely to live for > 6 months). Informed consent from the patient was needed. The TD entitled the patient to full reimbursement for drug expenses, reimbursement of expenses for equipment used in home care, and payment to informal caregivers. The TD has existed since 1990 and is well known by physicians, patients, and relatives.
Individual follow-up began 90 days before death or at the date of diagnosis (if it was less than 90 days before death) and ended at the date of death. For the TD, however, we could also collect the exact date of registration before the 90 days of follow-up. We first used the TD as a binary outcome variable and hence estimated the odds ratio (OR) of TD by logistic-regression models and calculated 95% CIs. In the models we adjusted for potential confounding factors. Age could be a confounder because elderly people may delay seeking medical advice for suspicion of cancer, and analogous to this we assume they may also delay seeking help in a terminal phase. Sex also must be considered a confounder because of different health service utilization by men and women, and type of cancer because different types of cancer have distinctly different natural courses of disease. Being married and having children are also possible confounders, because informal carers are able to ask for assistance and support in the health care system. As expected, we found a dependency between the odds of TD and week number before death, which we allowed for by including a separate constant for each week on which the risk of TD could depend. In the second analysis, we estimated the rate of admission to hospital for patients with a cancer diagnosis (a maximum of 12 weeks, accounting only for the time period after the diagnosis of cancer) by using TD as a binary covariate. Finally, we analyzed the risk of hospital death by logistic regression. All analyses were conducted by using STATA 8 (STATA Corp, College Station, TX).
RESULTS
For 34% of the patients in the total cohort (n = 3,445), the physician signed a TD (Fig 1). However, when survival time (ie, time from cancer diagnosis until death) was less than 1 month, only 8% received a TD. The declaration was signed a median of 52 days (interquartile range, 20 to 105) before death, with a mean of 100 days (95% CI, 91 to 110) (Table 1).
We found the probability of a TD to be significantly lower in the 70-year age groups and after eliminating patients living in a nursing home (n = 225). Female sex compared to male sex and hematologic cancers compared to "other" cancers showed significantly lower probability of a TD, whereas being married versus being single (widowed, divorced, or not married) and having cancer of the prostate or lung increased the probability of a TD (Table 2). Looking at the patients (n = 619) with short survival time ( 1 month), we found the same age distribution as in the total cohort. However, we found significantly fewer cancers with a known extended course (ie, prostate and breast cancers).
Looking at the effects of TD, we found that the admission rate increased less with TD (Fig 2). Interestingly, however, we found significantly longer admission time with TD (35.3 v 30.2 days). In our cohort, 56% (n = 1,935) died in the hospital, 28% (n = 965) died at home, 16% (n = 518) died in a nursing home, and 1% had an unknown place of death. Hospital death was found in 65% (n = 1,487) of cancer patients without TD, whereas only 39% (n = 448) of cancer patients with a TD died in the hospital. With a TD, the adjusted OR of hospital death was 0.25 (95% CI, 0.21 to 0.29).
DISCUSSION
A TD was signed for one third of terminal cancer patients. Significantly fewer elderly ( 70 years) and female patients were observed to receive a TD. An explicit terminal diagnosis seemed to reduce admission rates and reduced the risk of dying in an acute care setting.
This study has the strength of being a large population-based study in which the effect of selection bias is minimized because of the design of the cohort, which consists of all deceased cancer patients in a clearly defined time interval and a well-defined geographical area. The data collection was based on the complete population-based registries in Denmark, comprising uniform and identifiable information on deaths, hospitalizations, cancer development, and vital status. The personal identification number from the Danish Civil Registration Register ensures reliable record linkages of information. The validity of the Danish Cancer Register is high compared with other disease registers, and the National Discharge Register concerning the administrative data has been validated, showing an agreement of 98.5%.
However, there are some limitations to this study that deserve consideration. First, misclassification might have occurred by using the written declaration as a proxy for the terminal diagnosis. Because the TD carries with it benefits for reimbursement for expenses (medicine and equipment for home care), especially paid leave for informal caregivers, it may reflect more than simply the prognosis of the patients. For example, caregivers for the elderly (who may be old-age pensioners themselves) are less likely to benefit from paid leave from work. Although the declaration would have other advantages for such patients (and patients without a caregiver), they might be less likely to receive a TD. The TD, therefore, is most reliable as a proxy for a terminal diagnosis in patients with a positive TD. For patients without a TD, we cannot be sure that the physician did not make up his or her mind (diagnosing the patient as terminal). The physician may have made an implicit diagnosis. The administrative work of signing the declaration or patients considered without need of financial support might have held back the physician from signing a TD. In addition, the physician might weigh the advantages against the disadvantages of confronting the patient and the family with a terminal diagnosis. Studies have shed light on the existence of this bias. Collusion in doctor-patient communication has acted as a mechanism of delayed TD,32 and family physicians have been less willing to diagnose patients as terminal compared with other doctors.33 From the patient's point of view, patient coping strategies constrained an information-seeking behavior.34 Especially patients, but also informal carers, wish to maintain hope.35 Professionals, therefore, may have treated some of the patients without a TD as terminal patients. This type of misclassification may lead to some degree of underestimation of the effects of the terminal diagnosis. In another scenario, if the patient showed no sign of an approaching death, we could not expect the physician to sign a TD.36 However, when analyzing patient characteristics for receiving a terminal diagnosis, we analyzed at the point of death, at which we assume there ought to be signs of approaching death. In our analysis of the effects of terminal diagnosis, we broke down the total follow-up period into shorter intervals of time (weeks) and by this demonstrated an increasing effect as death approaches.
Not all patients dying from cancer will have the possibility of receiving a TD. Patients who died as the result of a potentially curative therapy, such as surgery or adjuvant or aggressive first-line chemotherapy, will probably not have been considered terminal. Those patients will probably die in an acute care setting, which in this study may overestimate the effect of terminal diagnosis. Such patients, however, are likely to be relatively few. The signed TD was collected from each municipal administration. Because of incomplete or missing information, we had to eliminate 13 small municipalities with a total of 941 cancer patients. However, those 941 patients were comparable to the rest of the cohort with regard to age, sex, marital status, children, and types of cancer. Finally, existence of some degree of misclassification in the registration system in the municipal administration must be considered. Misclassification caused by incomplete or erroneous registration in the municipal administration, however, is likely to be nondifferential with respect to the studied variables and in any case will tend to be reduced by the routinely conducted external auditing.
The risk of admission was initially higher among patients with a terminal diagnosis in the beginning of the 90-day period. We interpret this as being because of increased severity of the disease (ie, the more severe the illness the easier to detect a patient as terminal). If this interpretation is accurate, our results are even more important: Despite a more severe disease, patients with TD had fewer hospital admissions and more often died at home. The overall rate of hospital death in our study was similar to figures previously published for the US (56% v 52%).37
To our knowledge, only few population-based studies have analyzed patient-related factors associated with the physician decision about a terminal diagnosis. Hospice referral often implies more intensive treatment, and in North America the average patient stays less than 3 weeks in a hospice before dying.38 A diagnosis of "terminal stage" can often be made earlier, and the median period of survival after receiving a TD in our study was more than double (52 days). Many patients are not in need of intensive terminal care when they receive the TD. It is important to emphasize that a TD does not change the patient's overall rights in the Danish health care system; for example, the patient does not relinquish any acute care benefits as a consequence. In contrast, referral to a hospice may change the health care access for patient and family in the US Medicare program, which may have an influence on the timing of hospice entrance.39
In our study we found that fewer female and fewer elderly cancer patients received a terminal diagnosis even after adjusting for important confounders. The sex difference could be explained by the fact that women are still the primary caregivers in the family and hence are more proactive in getting the services needed for their spouse. That elderly patients are less likely to get a TD can be explained partially by the fact that elderly cancer patients are more reluctant to contact health care services, which can be seen by the relationship between increasing age and advanced stage of the disease at the time of diagnosis.40 From a health care service point of view, elderly patients ( 65 years) were less likely to receive cancer-related treatment,41 and physicians tend to undertreat pain in older patients.42 The elderly were also found to suffer delays in accessing terminal benefits,43 which correspond well with our results. As expected, short survival time (ie, time from cancer diagnosis until death) was found to reduce the proportion receiving a TD. Aggressive progression of the disease provides a reduced amount of time for the physician to detect a beginning terminal phase.
Our results, based on administrative databases, cannot elucidate mechanisms in doctor-patient communication or mechanisms in patient or doctor inner life. However, the use of administrative data can provide a practical and economical tool for profiling quality of care or screening for problems with care. For the health care providers, our studies show the importance of making the terminal diagnosis explicit. It is not surprising that an explicit terminal diagnosis facilitates planning of palliative care and thus has an effect on end-of-life care. Only 34% of the patients in our study received a TD. The late recognition of an approaching death might not allow healthcare professionals to discuss the feasibility of care and death at home. What is more important is that our results shed additional light on the probably insufficient services for some subgroups of end-stage cancer patients. Additional studies should focus on those groups to facilitate the necessary access to palliative care services.
Authors' Disclosures of Potential Conflicts of Interest
The authors indicated no potential conflicts of interest.
Acknowledgment
We thank G. Engholm and H.H. Storm from the Department of Cancer Prevention and Documentation, Danish Cancer Society, for inspiring input into the planning phase and access to data from the Danish Cancer Register. We also thank P. Pedersen from the Municipality of Odense for access to data from the Department for the Elderly and Disabled in Odense.
NOTES
Supported by the Health Insurance Foundation (Grants No. 2001B116 and 2002B025), the Danish Research Foundation for General Practice (Grant No. 586-193259), and the Danish College of General Practitioners' Foundation for Research in General Practice 2001.
Authors' disclosures of potential conflicts of interest are found at the end of this article.
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