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Diagnosis and Management of Lung Cancer: ACCP Guidelines (2nd Edition) |

Palliative Care Consultation, Quality-of-Life Measurements, and Bereavement for End-of-Life Care in Patients With Lung Cancer*: ACCP Evidence-Based Clinical Practice Guidelines (2nd Edition) FREE TO VIEW

John P. Griffin, MD, FCCP; Kathryn A. Koch, MD, FCCP; Judith E. Nelson, MD, JD, FCCP; Mary E. Cooley, RN, PhD
Author and Funding Information

*From the Division of Pulmonary, Critical Care, and Sleep Medicine (Dr. Griffin), Department of Medicine, University of Tennessee Health Science Center, Memphis, TN; the Division of Pulmonary and Critical Care Medicine (Dr. Koch), Department of Internal Medicine, University of Florida Health Science Center, Jacksonville, FL; the Division of Pulmonary and Critical Care Medicine (Dr. Nelson), Department of Medicine, Mount Sinai Medical Center, New York, NY; and the Phyllis F. Cantor Center for Research in Nursing and Patient Care (Dr. Cooley), Dana-Farber Cancer Institute, Boston, MA.

Correspondence to: John P. Griffin, MD, FCCP, University of Tennessee Health Science Center, 956 Court Ave, Room H314, Memphis, TN 38163; e-mail: jpgriffin@utmem.edu



Chest. 2007;132(3_suppl):404S-422S. doi:10.1378/chest.07-1392
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Objective: To develop clinical practice guidelines for application of palliative care consultation, quality-of-life measurements, and appropriate bereavement activities for patients with lung cancer.

Methods: To review the pertinent medical literature on palliative care consultation, quality-of-life measurements, and bereavement for patients with lung cancer, developing multidisciplinary discussions with authorities in these areas, and evolving written guidelines for end-of-life care of these patients.

Results: Palliative care consultation has developed into a new specialty with credentialing of experts in this field based on extensive experience with patients in end-of-life circumstances including those with lung cancer. Bereavement studies of the physical and emotional morbidity of family members and caregivers before, during, and after the death of a cancer patient have supported truthful communication, consideration of psychological problems, effective palliative care, understanding of the patient’s spiritual and cultural background, and sufficient forewarning of impending death.

Conclusion: Multidisciplinary investigations and experiences, with emphasis on consultation and delivery of palliative care, timely use of quality-of-life measurements for morbidities of treatment modalities and prognosis, and an understanding of the multifaceted complexities of the bereavement process, have clarified additional responsibilities of the attending physician.

Specific areas of interest were identified as important for the creation of American College of Chest Physicians guidelines for end-of-life care in patients with lung cancer.1 After a review of the medical literature revealed few prior guidelines, the improvement of communication between members of the health-care team and their patients and families was identified as essential. It was recommended that clinicians increase their focus on the patient’s experience of illness to improve congruence of treatment with goals and preferences of the patient. Education was considered inadequate at all levels of training despite an increasing availability of important information in this area. Effectiveness of advance directives was measured after examination of their legal development, and was found often to be lacking in critical medical situations, or inconsistent in their application. It was recommended that such instruments, valid and well understood by patients with lung cancer, should be present and applied as a physician responsibility. The hospital ethics committee was evaluated as to its clarification of ethical and legal matters, and assistance in resolution of difficulties between clinicians, their patients, their families and surrogates; although now available by requirement and sophisticated in its membership, the assistance of this group is seldom requested. The role of the critical care specialist in end-of-life care for patients with lung cancer was examined, including contributions to the treatment of reversible complications or comorbidity, and to palliative care. The role of the hospice environment for end-of-life care was measured and could be recommended as an appropriate choice in the longitudinal planning and care for these patients. Realization of the majority request for death in the home setting, the application of quality-of-life considerations, and satisfaction with the palliative care provided by the multidisciplinary team have resulted in progressively greater use of this environment.

To evaluate the role of palliative care consultation, quality-of-life measurements, and to broaden caregiver understanding of the bereavement process, a detailed examination of the English-language medical literature on these end-of-life care topics from a computerized database (MEDLINE) was performed by clinical researchers in these fields, covering the period of 1965 to 2005 identifying a majority of references in the past 10 years, but with use of classic psychosocial studies from other noncomputerized sources from earlier times. Additionally in 2006, several cancer-care Web sites were searched for even more recent unpublished pertinent information. Also, the authors of this chapter participated in extensive discussions of the experience of experts from multiple medical centers relative to these end-of-life topics. Recommendations were then developed by the writing committee, graded by the standardized method (see section on “Methods and Grading”) and reviewed by all members of the lung cancer panel, prior to approval by the Thoracic Oncology Network, Health and Science Policy Committee, and the Board of Regents of the American College of Chest Physicians.

Throughout the various stages of lung cancer, the needs of patients and their families are complex, with distress of all forms—physical, psychological, social, and spiritual—typically intensifying as the disease advances. Discussion of care goals as well as of symptom and treatment issues in the context of progressive illness is required. Arrangements for an appropriate care setting and adequate care giving support at the end of life require knowledge of available alternatives, and an experience-based understanding of how best to match needs and services. Many specialists in pulmonary disease are experienced in end-of-life care for patients with lung cancer, and appropriately consider this care to be an integral part of their work. However, the field of palliative medicine is emerging as a discrete specialty and a strong source of support for clinicians, for patients with serious and life-threatening illness, and their families. A growing body of evidence suggests that input from specialists in palliative medicine can improve the quality of patient care and reduce costs. Major professional organizations and consumer advocacy groups have called for better access to palliative care for patients with serious illness.24

Defining Palliative Care

Palliative care is interdisciplinary care to relieve suffering and improve quality of life for patients with advanced illness and their families.5The patient need not be imminently dying, or even certain to die of the illness, for this care to be appropriate and beneficial. Nor is palliative care a mutually exclusive alternative to curative care. In fact, effective palliation may be essential to enable the optimal delivery of aggressive, cure-oriented treatment. Increasing data document associations between symptom distress in lung cancer and other unfavorable outcomes including shorter survival610 and suggest, conversely, that effective palliative treatment is associated with favorable outcomes of cancer and other diseases.1114 Ideally, palliative care is initiated at the time of diagnosis of lung cancer or any serious or life-threatening illness, regardless of prognosis, and is integrated—“integrative palliative care”15—with restorative or life-prolonging treatments that are expected to benefit the patient. It is unfortunate, therefore, that many patients with severe illness including lung cancer still receive only repeated episodes of short-term, life-prolonging efforts, followed in the last weeks by a short period of end-of-life care in hospice or another setting.1617

Integrative palliative care is both patient centered and family centered. It is comprehensive, encompassing expert management of all forms of distress, communication about treatment plans and care goals, and facilitation of smooth transitions between care settings. The emphasis is on functional independence and quality of life at every stage of serious disease. Regular, formal assessment is used to identify problematic issues in a timely way, and an interdisciplinary team approach addresses the spectrum of needs of patients and families. This kind of care provides management throughout the course of serious illness, up to and including the end of life.

Growth of Palliative Care Programs in the United States

The past decade has been a time of explosive growth for the field of palliative medicine. A study18found that larger hospitals, academic medical centers, not-for-profit hospitals, and Veteran’s Affairs hospitals were significantly more likely to have a palliative care program. This development has been supported by growth in the numbers of certified palliative medicine professionals: physicians numbered nearly 2,000 and nurses numbered > 5,500 in 2005.19 Between 2000 and 2005, the number of postgraduate fellowships in palliative medicine more than tripled.1920 This period has also seen significant increases in the number of specialty journals and publications, and in research funding for palliative medicine.21Following recent co-sponsorship by seven major specialty boards, it is expected that palliative medicine will soon be formally recognized as a specialty of the American Board of Medical Specialties.22

Benefits of Palliative Care

Where palliative care is available, evidence suggests that involvement of this team will provide benefit to patients, families, clinicians, and health-care systems. Systematic reviews and metaanalysis of hospital palliative care programs showed improvement in symptoms and patient and family satisfaction, as well as lower rates of in-hospital death and shorter hospital length of stay.2326 A high rate of implementation of palliative care consultant recommendations, including symptom treatment, goal setting, and advance care and discharge planning, has been reported.27In addition, studies2829 suggest that as compared to conventional care, palliative care can achieve substantial reductions in direct and indirect hospital costs. These results have been observed across a range of hospital settings and clinical service delivery models. However, empirical studies to date were generally limited to single sites or programs, and lacked power to detect clinically significant differences in certain important outcomes including symptom management, analgesic prescribing, and service utilization. Many studies failed to use optimal statistical techniques to adjust for confounding variables and reduce bias in observational designs. Further research is needed to confirm benefits found in past studies of palliative care programs, and to define the essential components of successful interventions, so that existing and future programs can stand on a stronger evidentiary foundation.

Some institutions that do not have palliative care consultation services offer resources such as ethics services that may serve some palliative needs and achieve other favorable outcomes. In a large, multicenter, prospective, randomized controlled trial, Schneiderman et al30 compared ethics consultation with usual care for ICU patients in whom value-laden treatment conflicts were imminent or manifest that could lead to incompatible courses of action. The consultations followed a general process model attending to relevant medical factors, the patient’s known or inferred values and preferences, quality-of-life considerations, and other contextual factors. The consultant helped articulate consensus or disagreement and either facilitated implementing the consensus or facilitated ways to address and resolve the disagreement. Usual care in this study included family meetings or other conferences as judged appropriate by the health-care team. While mortality was not statistically different between the groups, length of stay for patients receiving ethics consultation was 3 days shorter in the hospital, and 1.4 days shorter in the ICU than for the usual-care patients. Nonsurviving patients in the intervention group also received fewer days of nonbeneficial life-sustaining treatment with mechanical ventilation. Patients, families, and clinicians found the consultations helpful in addressing treatment conflicts.

Defining a Role for Palliative Care Consultation

Input from palliative care consultants is not a substitute for close and continuing attention by pulmonologists and other clinicians to basic palliative needs. Whether or not specialty services are available, every physician and nurse (as well as respiratory therapists and others) caring for patients with lung cancer should receive education in the fundamentals of palliative care. This was the goal of the Educating Physicians in End-of-Life Care (EPEC) project sponsored by the American Medical Association and the Robert Wood Johnson Foundation, which has been widely disseminated.31A comparable program for nurses, the End-of-Life Nursing Education Consortium Project, was created by a partnership of the American Association of Colleges of Nursing and the City of Hope National Medical Center.32Cancer-specific educational resources are also available.3334 Through a collaboration between EPEC and the American Society of Clinical Oncology, the original EPEC curriculum is being adapted as “EPEC-O” to meet the specific needs of medical, surgical, and radiation oncologists.33 The National Comprehensive Cancer Network and American Society of Clinical Oncology have both developed guidelines for palliative care of cancer patients3334; and the National Consensus Project for Quality Palliative Care,35 a collaborative effort of five national palliative care organizations, has similar guidelines for patients with advanced chronic illnesses with or without malignancy. Readily accessible by the Internet, those recommendations can help to guide clinicians treating patients with all stages of lung cancer. As is the case for involvement of other specialists, palliative care consultation is most appropriate for complex or refractory problems. Conflict within families or between families and clinicians may require special skills and extended time for communication about care goals. Even without conflict, delivery of distressing news to patients and families in a clear and compassionate way is challenging for virtually all clinicians. Where multiple clinicians from different specialties are involved, palliative care consultants can facilitate consistent communication and care planning. Many physicians and others without specialized palliative care training find it difficult to coordinate the range of social and medical services required by patients with progressive disease and their families. Interdisciplinary palliative care teams provide assistance to clinicians and case managers as well as to patients and families in arranging appropriate transitions between care settings and engaging available services. Complicated grief or bereavement is also addressed by professionals with palliative care expertise.

Institution-specific factors including historical patterns, practices, and circumstances known as “culture” define different roles for palliative care services in different institutions.16 Some teams function almost exclusively as consultants, providing advice, support, and education to the primary team. In other institutions, the palliative care team may assume comprehensive, primary patient care responsibilities. The value of its input and the success of the palliative care team overall will depend on flexibility and adaptation to this institutional culture both by referring clinicians and by consultants. It will also be important for referring clinicians to remain actively involved with the patient and family as well as with palliative care consultants in all-important aspects of treatment, communication, and planning.

Building a Palliative Care Team

Although a growing number of American hospitals now have palliative care programs, the majority still do not.18 The benefits of these programs are demonstrable, but many palliative care services cannot fund themselves fully through clinical income and must rely to varying degrees on institutional and philanthropic support. Fortunately, excellent resources are available through the national Center to Advance Palliative Care (CAPC)36 to support all phases of program development, including step-by-step assistance in formulation of a persuasive initial proposal to the institution and a preliminary business plan. In addition, the CAPC provides practical information and tools for individual clinicians as well as larger teams to use in patient assessment and management, family support, and billing for palliative care services. Intensive hands-on training followed by an extended period of mentorship are available through the CAPC at six exemplary Palliative Care Leadership Centers across the country.19

Composition of the Palliative Care Team

The hospital-based palliative care team functions best as an interdisciplinary service,16 and Clinical Practice Guidelines of the National Consensus Project for Quality Palliative Care34 provide that specialist-level palliative care is delivered by an interdisciplinary team. Following the model of hospice, early palliative care teams in hospitals often consisted solely of clinical nurse specialists, but today, the hospital team in a large, tertiary institution includes a physician and social worker as well as the nurse specialist. Chaplains, bereavement counselors, and therapists are members of many teams, which may also include pharmacists and nutritionists. The National Consensus Project Guidelines provide that the team includes palliative care professionals with the appropriate patient population-specific education, credentialing and experience, and ability to meet the physical, psychological, social, and spiritual needs of both patient and family. Of particular importance is hiring physicians, nurses, and social workers who are appropriately trained and ultimately certified in hospice and palliative care.34 Valuable members and skills/experience requirements of a palliative care team are shown in Table 1 .

Maximizing the Benefit of Palliative Care Consultation

Patients appear to benefit most from care that combines appropriate life-prolonging treatment with palliation of symptoms, clear and sensitive communication, functional optimization, and caregiver support, across the trajectory of disease. Although direct empirical data are not yet available, clinical experience, expert opinion, and accumulating evidence suggest that the benefit of palliative care consultation is maximized by early engagement. This will require that referring clinicians as well as patients and families consider from the beginning the real prospect—always present in the context of lung cancer—of progressive disease and death. It will also require that they understand palliative care and curative/life-prolonging treatments as mutually enhancing rather than mutually exclusive. Traditionally, palliative interventions are often deferred until restorative treatment has clearly failed and death is imminent. This has also resulted in the use of burdensome and costly life-prolonging treatments when they are no longer beneficial, and in preventable suffering for patients at all stages of lung cancer. It is never too early for palliative care, and no patient or family facing lung cancer is “not ready yet.”

1. For all patients with advanced lung cancer (and their families), it is recommended that palliative care be integrated into their treatment, including those pursuing curative or life-prolonging therapies. Grade of recommendation, 1C

2. For patients with advanced lung cancer, it is recommended that palliative and end-of-life care include involvement of a palliative care consultation team, which should be made available. Grade of recommendation, 1C

Most lung cancers in adults are diagnosed at an advanced stage of disease when antineoplastic options are limited and palliative care assumes a central role.37 Palliative care aims to reduce symptoms, suffering and enhance health-related quality of life (HR-QOL) for patients and their caregivers.5,38These goals are pertinent for adults with advanced lung cancer and their health-care providers because the overall median survival is approximately 6 months despite advances in disease-oriented treatment.39 Thus, ongoing measurements of symptom distress and HR-QOL may provide assistance to clinicians in the following: (1) early recognition of problems, (2) identification of changes in symptoms over time in response to medical treatments and other interventions, (3) delineation of subgroups that may have unexpected worsening of symptoms and decreased HR-QOL, and (4) promoting discussion among clinicians, patients with lung cancer, and their caregivers, in making decisions about disease-oriented treatment, and about initiating appropriate palliative care services. This overview of the symptom experience and the associated effects on HR-QOL in patients with lung cancer discusses the role of symptom and HR-QOL assessment in the clinical setting, identifies the most common assessment instruments for use in adults with lung cancer, and reviews studies that have evaluated the effectiveness of symptom and HR-QOL assessment on improving clinical outcomes.

Several studies4042 have identified that patients with lung cancer experience more symptom severity and distress as compared with other samples of cancer patients. Elderly patients with lung cancer had a greater number of additional symptoms as compared to those with breast, colon, or prostate cancer.42 Adults with lung cancer had higher levels of symptom distress as compared with women with breast cancer, or men with genitourinary cancer in an ambulatory oncology setting.41

Adults with lung cancer often experience multiple symptoms that cluster and change with various disease-oriented treatments and over time.4347 The most common symptoms in patients with newly diagnosed lung cancer are fatigue, pain, cough, lack of appetite, and insomnia. Although many symptoms improve over time, fatigue and pain often remain as persistent symptoms. These two symptoms may also predict the number of other symptoms that patients experience. Of 841 elderly patients with breast, colon, lung, or prostate cancer, patients who reported both pain and fatigue had an average of 6.3 other symptoms, whereas those with fatigue alone had an average of 4.4 symptoms, those with pain alone had 3.8 other symptoms, and those with neither symptom had an average of 2.5 other symptoms.42 The most common symptoms experienced in adults with lung cancer near the end of life are presented in Table 2 .,4850

Patients with progressive lung cancer have a high prevalence of uncontrolled symptoms. Kreech and colleagues51found a median of nine symptoms among 100 adults with advanced lung cancer. Pain, fatigue, dyspnea, and anorexia were most common. The incidence and severity of dyspnea were highest in the lung cancer sample as compared to other advanced cancer patients.52 These findings suggest that most lung cancer patients suffer from multiple, dynamic symptoms that may benefit from ongoing assessment.

Similar to symptom distress, high rates of psychological distress and depression have been noted among adults with lung cancer. Zabora and colleagues53determined the prevalence of psychological distress among 4,496 cancer patients with 14 different cancer diagnoses. The prevalence rate ranged from a high of 43.4% among adults with lung cancer to 29.6% for adults with gynecologic cancers. Depression has also been reported at higher rates than the general population among persons with lung cancer, especially those with advanced stage disease,5456 and has been linked to decreased survival.57

Uncontrolled symptoms are associated with decreased HR-QOL and shortened survival.6,41,10,58Increased symptom distress was strongly associated with greater psychological distress and reduced quality of life in 243 cancer patients.59 In elderly adults with lung cancer, increased symptom severity was associated with increased levels of depression and a loss of physical and social functioning.6,58 Multiple studies10,41 have shown a link between symptom distress and length of survival. In 53 patients with inoperable lung cancer followed up for 3.5 years, postdiagnosis symptom distress was found to be the most important predictor of survival after adjusting for age, functional status, and personality traits.10 A subsequent study41 with 5-year follow-up confirmed these results, finding that increased baseline symptom distress scores in newly diagnosed lung cancer patients predicted decreased survival.

Similar to symptom distress, quality of life has also been shown to be a predictor of survival. Ganz et al60found that quality of life was related to length of survival in patients with advanced lung cancer. Median survival was 24 weeks for those reporting a high quality of life, compared to 11.9 weeks for those reporting a low quality of life. Montazeri and colleagues61 also found that prediagnosis global quality of life was the most significant predictor of length of survival in adults with lung cancer, even after adjusting for age and extent of disease.

In order to enhance clinical outcomes in this population of patients, the use of standardized questionnaires may be useful to monitor symptoms, enhance communication, and improve HR-QOL. The symptom experience is based on symptom occurrence, and distress.6264 Symptom occurrence includes frequency, duration, and severity of the symptom, whereas symptom distress is the degree of discomfort as reported by the patient in response to the specific symptom being experienced. To understand the complexity of the symptom experience among adults with lung cancer, multidimensional symptom assessment instruments may be useful, but instrument burden is an issue in certain settings. If a single symptom assessment measure is preferred, symptom distress will provide the most useful information.65

HR-QOL assessment is defined as the evaluation of health by using questionnaires that measure various domains, which include patient perception of symptoms, mental health, social factors, and functional status.66Increasingly, spirituality is also considered an essential component of HR-QOL in those with advanced disease.6770 Desired characteristics of HR-QOL assessment questionnaires include ease of self-administration, multiple dimensions, adequate psychometric properties, and efficacy in the particular patient population and setting in which they will be used.71

Because symptoms and quality of life are subjective experiences, patient self-reporting is the preferred method of assessment. Evidence suggests that disparity exists between patient and health-care provider perceptions of the patient’s symptom status and overall HR-QOL. Physicians tend to underestimate the severity of patient symptoms especially as severity of symptoms increase.72Similarly, physicians tend to underestimate overall quality of life in those with advanced cancer.73

For comprehensive assessment, it is recommended that at least three domains of HR-QOL be used. Several types of questionnaires are available to measure HR-QOL: generic, disease specific, cancer-site specific, and domain specific.68,74 Selection of a HR-QOL questionnaire depends on what one wants to measure and how one wants to use the results. Generic measures are not specific to any population and are useful when one wants to compare HR-QOL across populations. Disease-specific measures are designed for a certain group of patients such as those with cancer, cancer site-specific measures focus on a particular type of cancer, whereas domain-specific measures assess particular domains within the overall concept of HR-QOL. Disease-, cancer site-, and domain-specific measures are useful when one wants to monitor changes in an individual over time. A standardized pain questionnaire can help to monitor changes in an individual’s pain over time. The combined use of the various types of measures yields greater information about HR-QOL than any one type alone.

Advances have been made in the development and testing of HR-QOL questionnaires. Despite the fact that many of these instruments are brief, reliable, valid, and easy to use and score, the routine use of these questionnaires in clinical practice remains uncommon.7576 One problem limiting the use of symptom and HR-QOL assessment questionnaires in the practice setting may be the vast array of instruments that are available. Over 50 instruments have been used to measure quality of life in lung cancer studies.77 The instruments that have been used most often in adults with lung cancer are the Medical Outcomes Study 36-Item Short Form Health Survey (SF-36), the European Organization for Research and Treatment of Cancer Core-30 Item Quality of Life Questionnaire (EORTC-QLQ-30), Functional Assessment of Cancer Therapy-Lung Cancer (FACT-L), Lung Cancer Symptom Scale (LCSS), and the Symptom Distress Scale (SDS).37,7879 The SF-36 is a generic measure, the EORTC-QLQ-30 and FACT-L are disease-specific measures but also have cancer site-specific modules, the LCSS is cancer-site specific, and the SDS is domain specific (Table 3 ).84 Other symptom assessment questionnaires that have been used in adults with cancer are the Memorial Symptom Assessment Scale, Rotterdam Symptom Checklist, Edmonton Symptom Assessment Scale, and Hospital Anxiety and Depression Scale.8588

The development of questionnaires to measure HR-QOL in palliative care and end of life has received increased attention.69,71,8990 HR-QOL questionnaires that are used for patients receiving active treatment have several limitations when used in the care of those who have progressive disease and are dying. HR-QOL questionnaires that are used for cancer clinical trials often give increased weight to physical domains of functioning, whose salience may be decreased at the end of life. Moreover, many questionnaires used for clinical trials do not capture the existential and spiritual domain that often increases in importance as death approaches. To address some of these limitations, several questionnaires were designed to specifically measure HR-QOL at the end of life, which include the McGill Quality of Life Questionnaire, Hospice Quality of Life Index, and Missoula-VITAS Quality of Life Index (Table 4 ).94 A tool kit of instruments to measure end of life care is available and can be accessed at http://www.cher.brown.edu/pcoc/Quality.htm.89 For more in-depth discussion of the psychometric properties of these instruments, readers are referred to other sources of information.8083,9598

Use of Symptom and HR-QOL Assessment Questionnaires

In a review of the cancer literature, symptom and HR-QOL assessment interventions were defined as studies that administered a patient self-reporting HR-QOL questionnaire with the intent of using the results to improve clinical care. The growing number of studies99118 show that the use of these questionnaires is feasible in the clinical setting, and that both patients and clinicians have found them to be of potential value in enhancing the clinical encounter. Collective results showed that HR-QOL assessment improved some clinical outcomes but not others. Overall symptom distress and patient/health-care provider communication improved, but patient satisfaction and clinical management were not responsive to change.119 It appears that the systematic use of these questionnaires may be more effective for certain subgroups of patients (eg, cancer patients who were moderately to severely depressed at baseline had improved outcomes at 6 months).,110 In another study,114 the explicit use of HR-QOL data and discussion of pain and role function were associated with clinically significant improvement in HR-QOL.

Only three studies110,112113 addressed the use of these questionnaires as an intervention in lung cancer patients. Although encouraging, studies conducted to date have used quasiexperimental designs or have had small sample sizes, so larger, more rigorous studies are needed to evaluate the efficacy of systematic assessment within this group. Questionnaires may be especially helpful among lung cancer patients, who often experience higher rates of symptoms and psychological distress. Cooley and colleagues101 found that outpatients with advanced cancer undergoing specific treatment preferred symptom assessment questionnaires (ie, Symptom Distress Scale and Hospital Anxiety and Depression Scale), and disease-specific questionnaires (ie, FACT-L or European Organization for Research and Treatment of Cancer-Lung). The frequency of using the standardized assessment intervention varied from patients completing the questionnaire only once to completing it at every clinic visit.,110,112,114 Studies109,112,114 that administered the standardized assessment questionnaire on at least three consecutive clinic visits or on a monthly basis had significant improvement in patient outcomes.

Barriers to Implementation of Standardized Assessment in the Clinical Setting

Challenges exist in widespread adoption with recent evidence that HR-QOL assessment rarely occurs in clinical practice within the United States.76 Potential problems that may limit their use are lack of provider knowledge about application of HR-QOL data, lack of knowledge about the interpretation of HR-QOL scores, and logistical problems in data collection and recording.120 Now the SF-36 has extensive information about normative values, and data from adults with lung cancer can be compared with these values to understand the context and meaning for scores. Data have also been gathered about the use of the FACT, European Organization for Research and Treatment of Cancer, LCSS, and SDS questionnaires in adults with lung cancer, and reference values for symptom and HR-QOL domains are available.80,84,98,121123 Also, progress is being made in identifying a clinically meaningful change in scores. Cella and colleagues124 determined that a 2- to 3-point change in the lung cancer subscale and a 5- to 6-point change in the treatment outcome index of the FACT-L questionnaire constituted a clinically meaningful change in patients with advanced non-small cell lung cancer receiving chemotherapy during a clinical trial.

Another challenge is minimizing the logistical barriers with clinical resources often stretched to the limit in the current health-care environment. Successful strategies for implementation have been identified in feasibility studies. Wright and colleagues108 found that integrating these measures into the routine care of the clinic setting was successful, resulting in higher rates of patient completion over time. Automated data collection solved many of the logistical barriers. Patient acceptance of these methods of HR-QOL data collection was high. For further improvement, increased attention to the principles of effective dissemination, new information infrastructures and technologies, in combination with redesign of care76 are advocated.

3. For patients with advanced lung cancer, it is recommended that standardized evaluations with symptom assessment and abbreviated disease-specific HR-QOL questionnaires should be administered by the responsible member of the health-care team at the appropriate frequency. Grade of recommendation, 1B

The emotional pain of grief and bereavement has physical dimensions, particularly when the loss is sudden and unexpected, with survivors possibly experiencing substantial morbidity or mortality. Grief is the quintessential mind-body problem125; the nature of grief is that of a multidimensional loss.126 Even our terminology about death and bereavement creates a sensation of separation, loss, and change.

In caring for a person who has died, a physician’s role continues beyond the death itself.127That patient is a member of a family unit, and in compassionate care for the dying patient, the physician is also caring for the family. This should not end abruptly when the patient dies.128

Emotional tasks for someone who has been left behind include making sense of the death, finding meaning, restoring integrity, managing affect, managing emotions, and realigning relationships, including the relationship with the deceased.129132 How the survivor fares in their grief experience is related to how their loved one died, who the deceased was, who the survivor is, and what the relationship was. There is no medical literature specific to families of lung cancer victims, but the assumption is that there are elements of the survivor’s experience of grief that are common regardless of the diagnosis. As to closure, the sense is that the adjustment to grief must proceed at its own pace and, particularly for close family members, may be a life-long process.130,133134

Loss-attachment theory is commonly used to describe the emotional experience of bereavement.129 The survivor must revise internal models, and plans must change. Status, power, and control are often lost, and one’s very identity alters.129,131 The survivor must accept the reality of the loss on both intellectual and emotional levels, and adjust to an environment in which the deceased is missing.135

Engel136saw the process of mourning as a process of healing. In a small observational series137 of survivors with high risk factors for dysfunctional grief, several associations were noted that potentially contributed to personal growth as an outcome of grief. Such adaptive grief characteristics include the ability to see some good resulting from the death, having a chance to say goodbye, intrinsic spirituality, and spontaneous positive memories of the decedent.

Clinicians may be able to assist patients and families grieve in a more normal or “healthier” manner if they are able to facilitate adaptive grief by the following:

  • Giving sufficient forewarning for all parties that death is pending, providing the opportunity to at least begin to process the experience rather than being forced to face it suddenly. Anticipatory grief has not been shown to modify the experience of actual grief.129,131 This is rather a kindly warning to take special time together, to perhaps enable a discussion about life and death, which may give comfort to survivors.129,138

  • Providing adequate notice of imminent death so they can be present if possible because inability to be present at the death may lead to guilt.130,134135,139140

  • Making available palliative care to include focus on existential issues where appropriate141because problems in death experience can be associated with problems for the survivors.142

  • Honoring and respecting the cultural and religious practices of the patient and family because open-minded attitudes from clinicians can make the experience of death for survivors less traumatic.143144

  • Following up with survivors as a manifestation of caring, and to assess for any problems with the grieving process because some normal experiences of bereavement might in other situations be interpreted as signs of mental illness.129130,132,135,145

Sufficient Forewarning

Having a chance to say goodbye appears to be very important to survivors, and those who lose their loved ones suddenly and unexpectedly may show less resilience in recovery, and more anger and pain.130,134135,139140 Forewarning appears to improve adjustment during bereavement, particularly for widows.146147 The critical amount of forewarning necessary appears to be approximately 2 weeks.130,146

Forewarning creates some space for joint processing of the experience. Of parents in Sweden who had lost a child to cancer, none of the 147 parents who had talked with their child about death regretted it, but 27% of parents who did not discuss this regretted not having done so.138

Deaths that are expected are less likely to give rise to lasting psychological problems in the bereaved than those that are unexpected. In 2 years of follow-up of a series of sudden deaths, survivors who had no warning of potential loss subsequently had more sick days and larger number of psychiatric diagnoses than did a group of survivors with advanced warning.139

Psychiatric Difficulties and the Range of Normal

Both grief and clinical depression are syndromes that share constitutional symptoms such as sleep and appetite disturbance, as well as intense sadness, but in a grief reaction there is not the loss of self esteem that is associated with depression.135 Pharmacotherapy is useful for symptoms of true depression in survivors.148Formal grief counseling is not always helpful and should probably be reserved for those bereaved who truly appear to be dysfunctional.149150

The range of normal in bereavement embraces experiences that under other circumstances might be considered pathologic, and it may be helpful to reassure that these events are actually normal for the situation.129 Survivors may have a sense of the presence of the deceased (eg, many children feel watched over by their deceased parent for up to 2 years).,135 Transient hypnagogic hallucinations in which the deceased are seen or heard are reported by up to 50% of widows and may be misinterpreted as signs of mental illness.129 During this phase of yearning and searching, environmental cues can be perceived and interpreted as the actual presence of the deceased.132 Hearing or seeing a vision of a dead partner is culturally associated, and is mostly a pleasant experience.130 Of 14 men and 36 women in their early 70s during the first year of bereavement, a third of subjects experienced episodes of seeing the deceased, and half had illusions of feeling the presence of and of hearing and talking to the deceased.146

Existential Well-being

Nurture of spirituality may improve both the experience of death for the dying person and the bereavement experience of survivors. For Swedish parents discussing death with their dying children, discussion of existential issues such as the idea of life after death, affected quality of the dying experience for the family unit.138 Spirituality, as well as but distinct from religious beliefs,141 may contribute to well-being and coping strategies.151

Successful palliative care enables a dying person to adapt to the situation and find quality in the existential, spiritual, psychological, and social domains despite the decline in physical and functional domains. The assumption is that improved patient adaptation to the experience of dying may help the survivor in adaptation to the loss. In two small studies of terminally ill cancer patients, scores of existential well-being correlate with physical well-being and psychological symptoms despite physical pain,151and depression and hopelessness were inversely related to spiritual well-being.152 In a group of 1,610 ethnically diverse cancer patients, spirituality was shown to have a positive association with quality of life affecting it as much as physical well-being.70

Spiritual beliefs have been shown to be important in predicting clinical outcome for dying patients,153in management of death distress,154and in occurrence of end-of-life despair.155The presence of religious beliefs may reduce dependence on health professionals by cancer patients as they are dying.156One study157 looked at how spiritual beliefs in survivors may assist in adaptation to loss, but no study has yet examined how nurturing spiritual belief and existential comfort in the dying patient might help the survivor.

Rituals for Death and Dying

Culture influences the meaning and experience of death and dying as well as mourning practices.158For the sake of both the deceased and the survivors, religious rituals of death should be honored.159 Physicians need to maintain a nonjudgmental attitude toward unfamiliar beliefs and practices and be willing to negotiate and compromise when world views conflict.143 Mourning is culture based, what Parkes129 called “the social face of grief.” Customs, rituals, and how that family functions as a subunit of its culture all introduce variables.159 Misunderstandings can develop from the simplest differences in body language, custom, or address. Human touch demonstrates respect for grieving Latino individuals,159but Chinese do not usually like to be touched.160 Sending cut flowers is not part of the Jewish tradition.159 Laotian elders believe that their “death date” is predestined; if you talk about death, you are tempting fate, a taboo that is common to all Southeast Asian cultures,161 yet is in direct conflict with the recommendation that the clinician be open and honest about impending death. Several countries believe that each person has several souls, regional variation ranging from 3 to 32 souls.158

In a study by the Connecticut Coalition to Improve End of Life Care, 95 participants identified 10 domains that characterize the quality of the death experience, and only 1 domain related to physical distress. Minority participants were concerned that spiritual aspects of dying are not adequately addressed currently, that there is insufficient respect and tolerance for cultural and religious differences, and that respect for each death as a unique and individual phenomenon is lacking.144

Bereavement is a family developmental process that unfolds in cultural context.162 Prevailing North American attitudes toward practices of other cultures can be very narrow minded, particularly the attitude that recovery is associated with successful detachment from the dead.162 Geissler160 notes that concepts of health, illness, and care cannot readily be separated from general cultural values, beliefs, and practices; many of the tenets of conventional medicine and role expectations during the patient-provider encounter are derived from a Northern European world view that espouses individualism, independence, paternalism, reductionism, and belief in the scientific methods of finding truth.

Historically, Freud’s163work in 1917 compared the emotions experienced in mourning to those of melancholia, and Lindemann164 in 1944 described the experience of 101 bereaved who had lost their loved one in a night club disaster, coining the concept of morbid grief characterized by somatic distress, preoccupation with the image of the deceased, guilt, hostility, and loss of patterns of conduct.

The identification of pathologic, complicated, morbid, or traumatic grief may be difficult due to a wide spectrum that probably qualifies as normal grief,6,43 which is a self-limiting process consisting of sadness, longing for the deceased person, somatic complaints, and subsequent recovery.134

Physicians should not impose their own notions about what is healthy or unhealthy grief but should reference the assumptions of the culture/subcultures about good and bad, and health and sickness.162 Although there is no specific time frame for failure to adapt to loss that signals impaired grief, specific symptoms may be used as discriminators to identify abnormal reactions to loss134: negative perceptions of self, functional impairment, profound depression, suicidal ideation, and pervasive feelings of worthlessness. In 112 participants after bereavement, Ott165 identified 29 participants with complicated grief as early as 6 months after loss; this group had more additional life stressors, perceived less social support, and achieved less improvement. Survivors with previous psychiatric histories, low self esteem or poor coping skills, high levels of dependency on the deceased, and abuse/trauma histories are high risk. There is also a category of “high distress” that may be identified early in bereavement: high levels of depressive, anxiety, anger, or rumination symptoms are associated with high intensity of grief reaction at the outset and correlate with poor 2-year outcome.149 A randomized controlled trial166 in treatment techniques for individuals with complicated grief indicates that combining techniques for treatment of posttraumatic stress disorder with standard interpersonal therapy techniques used for depression may improve grief scores to a greater degree and with faster response times than use of techniques to treat depression alone.

There may be physical as well as psychological morbidity, such as increased morbidity in cardiac events, hypertension, cancer, suicidality, changes in food, alcohol and tobacco intake, and constitutional complaints at the 6-month point following loss.167168 Palliative care and hospice care services may not only help the dying patient but may also improve both psychological147 and physical169 bereavement outcomes.

Medical Morbidity of Grief

There appears to be an overall increased risk of premature death for survivors in the years immediately following the death of a spouse.127,170 The bereaved are probably at greater risk of death especially in the first year of their loss, and men are at greater risk, but the risk remains small in absolute terms.131,171179 Christakis and Allison170 have shown that not only is there increased risk of death following death of a spouse, there is even increased risk following hospitalization of a spouse. Caregiving itself, during the patient’s illness and decline, is an increased risk factor for mortality, particularly when the caregiver experiences strain.180

The physiologic stress created by the impact of loss has been associated with altered autonomic, immune, and endocrine response.181184 The connection between disrupted sleep and depression of the immune system was made by Irwin et al.185Normal sleep patterns at 6 months following loss of a spouse correlate with better emotional health and energy a year later.186 Consistent exercise at least once a week and consistent attention to appropriate caloric intake correlate with better health in survivors as well.186 One of the goals in future research about bereavement is to develop a stronger identification of possible cause-and-effect relationship between the experience of loss and physiologic immune and/or neuroendocrine changes that may alter medical outcome.125

Practitioner Intervention

Practitioners can contribute to the recovery of bereaved family and friends of their dying patients in a number of different ways:

  • Make decisions early about how to face impending death, notifying the patient and family that hopes need to be altered and changing circumstances need to be adapted to.

  • Provide the patient as much support in the dying process as possible: access to the support systems that are provided may help family as well as patient.

  • Provide the opportunity for family to be at the bedside when death occurs if possible.

  • Focus on the family as well as the patient during the death.129

  • Enquire into cultural rituals and beliefs in death and dying.158160,187

  • Accept as normal those experiences of survivors that entail visitations of the departed.

  • Identify those survivors at risk for correct referral because among many studies of interventions with positive outcomes there have been observations of treatment-associated deterioration.149150

  • Encourage maintenance of healthy lifestyle during the period of caregiver burden as well as during bereavement.186

The Institute of Medicine in 1984 indicated its belief that health professionals, having become involved with the families of dying patients prior to the death, have some obligations to these families after the death.127 Follow-up or some condolence contact by caregivers appears to be a particularly comforting note for the bereaved.133134,140,188190 Failure to communicate conveys a lack of concern about the loss.190 Follow-up also enables diagnosis of potentially maladaptive mourning.128 Some follow-up is indicated, even if purely for social-emotional reasons.191 There may be unanswered questions.140 Contact after death reassures the survivor that something more than mechanical medicine had been given.130

In a study146 of 78 widows and 41 widowers, physicians of lost spouses had disappointed 33% of widows and 27% of widowers. Primary issues were allegations of failure to be honest; avoiding the family; lacking gentleness; having a poor bedside manner; being cold, impersonal, or unconcerned; and misdiagnosing the disease. Characteristics of physicians who offered great help to surviving spouses included honesty, compassion, availability, and an unhurried and comforting manner.146

The clinical tools to avoid such disappointment are basic communication skills such as active listening, joint reflection, empathy, setting limits, and clarification of the emotions being experienced.134 In particular, the clinician can provide reassurance about the normality of grief or simple explanations of any symptoms.129

Clinician

The grief experience of clinicians is similar to that of loved ones, in quality if not in severity,192but the term disenfranchised has been applied to the grief of clinicians because it seems somehow less legitimate than the grief of family and friends.193 There are additional challenges that involve issues of professional maturity,194competence, integrity, and interprofessional friction that may contribute to special difficulties for clinicians.195 Of particular note is the tendency of clinicians to blame themselves for imagined failures; grief may be more intense if it is believed that the death was preventable.195

For oncology nurses, work stresses influence nursing burnout.194,196 Nurses who face their own mortality and recognize their own reactions without defensiveness can cope constructively.196 Informal surveys of bereavement workshops suggests that most nurses feel they manage their own grief more effectively if they help the patient die a good death.194

In a study of the physician’s emotional reactions to the death of a patient in two US academic hospitals, 74% of physicians reported satisfying experiences in the care of 68 dying patients.197 Women physicians and those physicians who had cared for their patients for a longer period of time tended to have stronger emotional reactions to the death of their patient. Less than one fourth of interns and residents found that their faculty were helpful in providing them emotional support.

It is as important for physicians as it is for family members to accept the normalcy of their own feelings of bereavement. Physicians should be alert to their own emotional reactions and take care to name and embrace their strong feelings because failure to do so may promote distress, disengagement, burnout, and poor medical judgment.198It has been shown that strong personal reaction may be deleterious in emotionally charged situations.199

With respect to death and dying issues, lack of self-awareness by clinicians regarding their own feelings about life-sustaining medical technology, death, and disability may contribute to inappropriate prescription of such technology; there may be failure to face the difficult decisions directly about appropriateness, particularly if there are high levels of ambiguity and uncertainty.198

If a physician has emotional discomfort with end-of-life issues, it may also inhibit effective handling of patient and family interchanges on death, dying, and bereavement issues. Physicians may feel awkward in discussing emotionally charged topics of such an existential nature, but learning how to respond effectively to the patient’s and family’s religious and spiritual concerns may help everybody, including the clinician, to find comfort and closure.200201

Burnout, however, can be associated also with insufficient training in communication.202 If, through practice and experience in caring for the dying and their families, specific rewards can be identified by the practitioner, distress caused by grieving for a patient’s death can become more acceptable191,203 and become a source of professional reward.191

Clinicians must develop a delicate balance between emotional involvement and detachment. Considering the multidimensional impact in the loss of a patient, Parkes129 suggests that we examine our own mortality by asking ourselves, “Is today a good day to die?”

4. It is recommended that clinicians of patients who die from lung cancer should extend communication with the bereaved family and friends after death. Grade of recommendation, 1C

5. For patients with lung cancer, proactive interventions, such as those listed below, are recommended to improve grief outcomes: (1) informing the patient and family of foreseeable death within weeks; (2) forewarning family of impending death; and (3) enabling effective palliative care, focused on spiritual, existential, physical, and practical concerns. Grade of recommendation, 1C

6. It is recommended that clinicians of dying patients with lung cancer encourage caregivers to maintain a healthy lifestyle during the period of caregiver burden, as well as during bereavement. Grade of recommendation, 1C

7. It is recommended that clinicians of patients dying from lung cancer honor rituals of death and mourning in a culturally sensitive manner. Grade of recommendation, 1C

Palliative care consultation and expertise should be available for patients with lung cancer from the time of diagnosis and planning of primary modes of attempted curative therapy until their demise. This multidisciplinary team should be utilized for the application of supportive care modalities for the patient, family, and caregivers. The leader of this team could be a newly recognized and credentialed subspecialist in internal medicine. HR-QOL measurements are of clinical importance in the continuous assessment of symptomatic distress in these patients throughout the course of their disease, which permits the earliest and most beneficial application of specific palliative therapy. Bereavement identifies an additional attending physician responsibility in considering the physical and emotional needs of family members and caregivers before, during, and after the death of their loved one.

1. For all patients with advanced lung cancer (and their families), it is recommended that palliative care be integrated into their treatment, including those pursuing curative or life-prolonging therapies. Grade of recommendation, 1C

2. For patients with advanced lung cancer, it is recommended that palliative and end-of-life care include involvement of a palliative care consultation team, which should be made available. Grade of recommendation, 1C

3. For patients with advanced lung cancer, it is recommended that standardized evaluations with symptom assessment and abbreviated disease-specific HR-QOL questionnaires should be administered by the responsible member of the health-care team at the appropriate frequency. Grade of recommendation, 1B

4. It is recommended that clinicians of patients who die from lung cancer should extend communication with the bereaved family and friends after death. Grade of recommendation, 1C

5. For patients with lung cancer, proactive interventions, such as those listed below, are recommended to improve grief outcomes: (1) informing the patient and family of foreseeable death within weeks; (2) forewarning the family of impending death; and (3) enabling effective palliative care, focused on spiritual, existential, physical, and practical concerns. Grade of recommendation, 1C

6. It is recommended that clinicians of dying patients with lung cancer encourage caregivers to maintain a healthy lifestyle during the period of caregiver burden, as well as during bereavement. Grade of recommendation, 1C

7. It is recommended that clinicians of patients dying from lung cancer honor rituals of death and mourning in a culturally sensitive manner. Grade of recommendation, 1C

Abbreviations: CAPC = Center to Advance Palliative Care; EORTC-QLQ-30 = European Organization for Research and Treatment of Cancer core 30-item quality of life questionnaire; EPEC = Educating Physicians in End-of-Life Care; FACT-L = functional assessment of cancer therapy–lung cancer; HR-QOL = health-related quality of life; LCSS = Lung Cancer Symptom Scale; SDS = symptom distress scale; SF-36 = 36-item short-form health survey

The authors of this article have no conflicts of interest to disclose.

Table Graphic Jump Location
Table 1. The Palliative Care Consultation Team
Table Graphic Jump Location
Table 2. Highly Distressing Symptoms in Lung Cancer Patients Within 90 Days of Death
* 

Defined as symptoms score ≥ 3 on the SDS (n = 42).

Table Graphic Jump Location
Table 3. Comparison of Key Characteristics of HR-QOL Measures for Patients With Lung Cancer*
* 

EORTC-QLQ-LC13 = European Organization for Research and Treatment of Cancer-Quality of Life Questionnaire-Lung Cancer.

Table Graphic Jump Location
Table 4. Comparison of Key Characteristics of HR-QOL Measures for Patients With Progressive Disease/End of Life
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Figures

Tables

Table Graphic Jump Location
Table 1. The Palliative Care Consultation Team
Table Graphic Jump Location
Table 2. Highly Distressing Symptoms in Lung Cancer Patients Within 90 Days of Death
* 

Defined as symptoms score ≥ 3 on the SDS (n = 42).

Table Graphic Jump Location
Table 3. Comparison of Key Characteristics of HR-QOL Measures for Patients With Lung Cancer*
* 

EORTC-QLQ-LC13 = European Organization for Research and Treatment of Cancer-Quality of Life Questionnaire-Lung Cancer.

Table Graphic Jump Location
Table 4. Comparison of Key Characteristics of HR-QOL Measures for Patients With Progressive Disease/End of Life

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