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Symptom Prevalence, Intensity, and Distress in Patients With Inoperable Lung Cancer in Relation to Time of Death

Carol Tishelman, Lena-Marie Petersson, Lesley F. Degner, Mirjam A.G. Sprangers

From the Department of Neurobiology, Care Sciences and Society, Division of Nursing, Karolinska Institutet; Research and Development Unit, Stockholms Sjukhem Foundation, Stockholm, Sweden; Department of Medical Psychology, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands; University of Manchester, School of Nursing, Midwifery and Social Work, Manchester, United Kingdom; and the Faculty of Nursing, Helen Glass Center for Nursing, University of Manitoba, Winnipeg, Manitoba, Canada

Address reprint requests to Carol Tishelman, PhD, RN, Research & Development Unit, Stockholms Sjukhem Foundation, Mariebergsgatan 22, 112 35 Stockholm, Sweden; e-mail: carol.tishelman{at}ki.se

	ABSTRACT

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Purpose To examine symptom prevalence, intensity, and association with distress in patients with inoperable lung cancer (LC), using time to death as point of reference.

Patients and Methods A consecutive sample of 400 patients completed the European Organisation for Research and Treatment of Cancer Quality of Life Questionnaire C30 plus a 13-item LC-specific scale and the Thurstone Scale of Symptom Distress–Lung Cancer at six time points during the first year after diagnosis. Patients were divided into subgroups, using data from the time point closest to death (< 1; 1 to 2; > 2 to 3; > 3 to 6; > 6 to 12; and > 12 months before death) for analysis.

Results More than 50% of patients in all subgroups reported problems related to physical, role, and emotional functioning; fatigue; dyspnea; and cough. In general, functional levels were lower and symptoms higher in subgroups closer to death. Notably, clinically relevant differences were also found in role and social functioning and appetite loss between the two groups furthest from death. A consistent pattern was found among the six subgroups, with breathing, pain, and fatigue rated as the symptoms most associated with distress.

Conclusion High prevalence of symptoms was found in all subgroups, with higher intensity in subgroups closer to death, indicating a need for prophylactic and proactive symptom management. Less concordance was found among symptom prevalence, intensity, and association with distress in subgroups further from death. Future studies should investigate longitudinal associations between symptoms with low intensity and high distress, and examine their clinical implications.

	INTRODUCTION

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The majority of lung cancer (LC) patients are diagnosed with advanced, nonresectable disease, with less than 40% surviving the first year postdiagnosis.¹ This poor prognosis is coupled with severe symptomatology from diagnosis onward,² with a wide range of physical and psychological symptoms resulting from disease progression and treatment-related adverse effects.^3-5 Fatigue, pain, and dyspnea have been identified as common symptoms associated with particular distress in LC patients.^2,6-8 Zabora et al⁹ also noted high levels of psychological symptoms in this patient group, with 43% of LC patients reporting psychological problems compared with approximately 35% of patients with 13 other cancer diagnoses.

The need for evidence-based palliative care to support the patient's quality of life (QOL)¹⁰ is thus prominent for patients with nonresectable LC throughout the disease trajectory. Standardized health-related QOL (HRQOL) questionnaires are important tools for obtaining such data. One major hindrance in attaining high-quality and clinically relevant data is "functional attrition"¹¹ compromising longitudinal studies of HRQOL, as LC patients become too ill to complete questionnaires, often dying during follow-up. Several studies address this problem in patient populations with mixed cancer diagnoses by relating HRQOL scores to time of death. ^12-15 Framing data in relation to the course of disease rather than by researcher-determined time points can increase clinical relevance.

Although studies of HRQOL often focus on frequency or intensity of symptoms, Tishelman et al⁸ recently found that the dimensions of symptom intensity and symptom distress were not equivalent in LC patients. They argue that data reflecting patient interpretations and prioritizations of their symptom experiences, such as assessments of distress, provide an important complement to assessments of symptom frequency and intensity.

In this study, three different dimensions of symptom experience are examined: symptom prevalence, intensity, and association with distress in a naturally occurring sample of patients with inoperable LC, using time to death as point of reference. The specific questions addressed are (1) What is the prevalence of reported symptoms in relation to time to death? (2) What is the intensity of reported symptoms in relation to time to death? and (3) What are the relative patterns of distressing symptoms in relation to time to death? The overall objective is to provide clinically relevant data, to ensure that efforts to improve symptom management accommodate patient perspectives.

	PATIENTS AND METHODS

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Patients and Procedures
These data derive from a longitudinal study of 400 patients with primary inoperable LC recruited between April 1998 and October 2002. Patients able to communicate adequately in Swedish were recruited consecutively through the lung medicine departments of two university hospitals in Stockholm soon after diagnosis (mean, 31 days; median, 24 days). These hospitals are the primary centers for nonsurgical LC treatment in the region. After treatment, continued care varies greatly with regard to setting and extent of contact with the health care system. The project was approved by the Research Ethics Committee.

Staff at both departments were asked to give the patient a first information letter, with a copy also sent to patients' homes. Thereafter, a research nurse contacted the patient to obtain informed consent for study participation and answer any further questions. The patient decided where the interview would be held (eg, at home, in the hospital clinic, or in the ward). Data were collected in the presence of a research nurse who could clarify the instructions if needed. Participants were offered a 50 sek (approximately 5.3 or $6.25) gift certificate donated by COOP Sweden (a national federation of cooperative stores) at the conclusion of each interview.

Patients completed a set of questionnaires assessing HRQOL and symptom experience at six time points: close to diagnosis and before beginning treatment; after 2 weeks; and 1, 3, and 6 months; and 1 year after the first assessment. The time point for data collection closest to time of death completed by each participant was used for the analyses presented here.

Questionnaires
EORTC QLQ-C30 and LC13. In this study, 28 of the 30 items of the European Organisation for Research and Treatment of Cancer Quality of Life Questionnaire C30 (EORTC QLQ-C30, version 3.0), a cancer-specific HRQOL questionnaire,¹⁶ are utilized. Five scales assess physical, role, emotional, cognitive, and social functioning. Three symptom scales assess fatigue, nausea and vomiting, and pain, and six single items measure dyspnea, insomnia, appetite loss, constipation, diarrhea, and financial difficulties. The 13-item LC-specific module, the EORTC-LC13¹⁷ was also administered. One scale assesses dyspnea, and the remaining single items assess coughing, hemoptysis, sore mouth, dysphagia, peripheral neuropathy, alopecia, and pain (in chest, arm or shoulder, or other parts of the body). Four response options are employed (not at all = 1, a little = 2, quite a bit = 3, and very much = 4). Scores of both questionnaires were linearly transformed to scales of 0 to 100.¹⁸ Higher scores represent higher levels of functioning and/or symptomatology. Although items do not distinguish among intensity, frequency, or severity of problems, mean scores are interpreted as reflecting intensity of functioning and symptoms. The EORTC QLQ-C30 and LC13 have been found to yield adequate levels of reliability and validity in Swedish.^17,19

TSSD-LC. A Thurstone scale of pairwise comparisons of symptoms associated with distress, the Thurstone Scale of Symptom Distress–Lung Cancer (TSSD-LC), was developed and pilot tested^8,20 before use in this study. Nine commonly occurring symptoms in patients with LC (appearance, appetite, bowel function, breathing, cough, fatigue, insomnia, outlook, and pain) were selected based on an earlier Canadian study²¹ and reconfirmed as appropriate in a Swedish pilot study.²⁰ The nine symptoms are arranged in pairs of all possible subsets of two, yielding 36 pairs. The symptoms were presented to the patient as a set of cards with one symptom pair per card, with card order determined using the Ross matrix of optimal ordering²² to avoid selection bias. For each symptom pair, patients were asked to select the symptom they believed to be associated with most distress for them, irrespective of the occurrence of those symptoms at present. The number of patients who prefer Symptom 1 to Symptom 2, Symptom 1 to Symptom 3, and so on, yields preference frequencies. These frequencies are divided by the number of patients responding to calculate the percentage of the sample that prefers each symptom to every other symptom. These proportions are then translated into standard normal scores for each item, with scores varying between –3 and +3. The more patients who select one symptom in a pair over the other, the greater the preference for that symptom, and the higher its score. Thus, higher scores indicate more distress associated with a symptom.²³

Demographic and Medical Data
Data on LC type, disease stage, and treatment were collected from the Regional Cancer Registry.

Data Analysis
In the present study, all 400 patients were divided into subgroups based on length of time between their last interview and death. Six subgroups were formed: less than 1 month before death (n = 57), 1 to 2 months (n = 65), more than 2 to 3 months (n = 72), more than 3 to 6 months (n = 87), more than 6 to 12 months (n = 52) and more than 12 months (n = 67) of survival postinterview. These time points were chosen to maximize specificity close to death, while allowing for comparability with other studies examining symptomatology and HRQOL in relation to time of death.^12-15 These divisions also resulted in relatively comparable sample sizes among subgroups. As seen in Table 1, no statistically significant differences (P < .05) were found in sociodemographic characteristics, disease stage, and LC type across subgroups, nor were significant differences found in the distribution of treatment within the 3 weeks before interview. However, significant differences were found across subgroups in the distribution of treatment received at any time postdiagnosis, reflecting clinical reality.

The intensity of functioning and symptoms was assessed by mean values and standard deviation. When calculating mean scale scores, the 42 individual items missing (1.3%) were imputed in accordance with recommendations.¹⁸ Differences in mean scores between the six subgroups were tested with analysis of variance (ANOVA). A P value less than .05 was considered statistically significant. A difference of more than 10 points between mean scores was considered clinically meaningful.²⁴

The relative ranking of distressing symptoms was calculated with the TSSD-LC. Nineteen patients had not responded to the TSSD-LC, and five additional patients were excluded from this analysis because of six or more missing values. The internal consistency of the TSSD-LC was identified by calculating the number of circular triads or inconsistencies in each participant's responses, with 27.24 circular triads indicative of statistically significant inconsistencies.²³ Only one respondent was found to be inconsistent in his or her response (29.5 circular triads), with no other respondent having more than 26.00 circular triads. The mean number of circular triads among the respondents was 3.13 (range, 0 to 29.50). Kendall's coefficient of agreement, used to measure the degree of consistency in ranking among patients, was 0.25 to 0.31 for all subgroups, indicating low to moderate agreement among patients as to the overall ranking of the symptom. A score of 1.00 would represent complete agreement among respondents.

	RESULTS

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Four hundred of the 910 patients informed about the study (44%) participated (Fig 1). Most nonparticipants declined without specifying a reason (n = 148) or said they were too tired to participate (n = 126). Nonparticipants were older than participants (mean age, 68.8 v 64.5 years; P < .0001) with shorter survival times (mean survival, 263 v 320 days; P = .001), but were not significantly different with respect to sex. Study participants also differed from population data from newly diagnosed patients with nonresectable LC during the same time period in the Stockholm-Gotland Cancer Registry. The registry population was older (n = 2,375 patients; mean age 68.8) with shorter survival (n = 1,975 patients, mean survival = 178 days) than study participants. These differences may be caused in part by registration of patients from nonuniversity hospital settings at late stages.

View larger version (11K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 1. Flow chart of participation.

The total sample (N = 400) was almost equally divided between men (52%) and women (48%; Table 1). Women were significantly younger than men in the entire sample (mean age, 62.6 v 66.2 years; P < 0001). Eighty-five percent of patients had non–small-cell LC (NSCLC), a prevalence rate similar to Swedish national data.²⁵ Seventeen percent of the patients were deemed inoperable because of tumor localization or comorbidity rather than disease stage.

Prevalence of Reported Symptoms in Relation to Time to Death
The problems reported by more than 50% of patients in all subgroups were related to physical (items 1, 2, and 4), role (items 6 and 7) and emotional functioning (items 22 and 24); fatigue (items 10, 12, and 18); and dyspnea (item 8; Table 2). In the subgroup closest to death, more than 50% of patients reported problems in 24 of 28 QLQ-C30 items. More than half of the patients in all subgroups reported problems on the LC13 items related to dyspnea (items 4 and 5) and cough (item 1; Table 3).

Relative Pattern of Distressing Symptoms in Relation to Time to Death
Table 4 illustrates the relative ranking of distressing symptoms according to the TSSD-LC in the subgroups. There is a consistent pattern with breathing, pain, and fatigue ranked as the symptoms associated with most distress in all subgroups. The scores indicate that the association between problems with breathing and distress is well differentiated from other symptoms in all subgroups, except the subgroup 2 to 3 months before death. In this subgroup, pain and breathing problems are nearly equivalent in their association with distress. Appearance is ranked lowest in all subgroups. Although there is some consistency in ranking order even among other symptoms, they are less differentiated in terms of the magnitude of their relative ranking, tending to be clustered in the middle of the scale.

	DISCUSSION

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As expected, symptomatology was higher in subgroups closer to death, although the relatively high prevalence of symptoms even in patients surviving more than 1 year after interview is notable. Reports of symptom prevalence in advanced LC are relatively rare, whereas symptom intensity is more commonly reported.^26,27 However, direct cross-study comparison is hindered by differences in clinical features of samples employed, differences related to care provision, differences related to time point on the sickness trajectory, and the wide variety of assessment measures and strategies. Moreover, even comparison with EORTC QLQ-C30 reference values²⁸ is hindered because these are not specified by time point in the disease trajectory.

This analysis indicates that the dimensions of symptom prevalence, intensity, and distress are not equivalent, but provide complementary information of clinical importance. Previous investigation of these patients indicated that breathing, pain, and fatigue were also consistently ranked as associated with most distress in subgroups based on time from diagnosis, sex, age, and type of LC.⁸ Hence, the order of the symptoms associated with most distress is robust in these patients with inoperable LC.

Difficulties in breathing were generally ranked as most distressing among these patients. However, the clear differentiation between breathing and pain is particularly evident in the subgroup with longest survival postinterview, and least evident in subgroups with 3 to 6 months, 2 to 3 months, and 1 to 2 months to death. It is interesting to note that, despite differences in research approach and patient group, Strömgren et al²⁹ found similar prioritizations in patients with heterogeneous cancer diagnoses in palliative care. Pain was the most prioritized symptom, followed by physical function, dyspnea, and fatigue. Interestingly, Strömgren et al²⁹ found that the prioritization of symptoms was closely associated with actual symptom reports in their sample of patients close to death. This is also the case in our sample, in which the symptoms consistently associated with most distress are also those reported as most prevalent and among the most intense close to death.

Earlier in the disease trajectory, distress is less concordant with prevalence and intensity in this study. On the basis of qualitative data, it has been demonstrated that respondents to the TSSD-LC incorporate past and current experiences, as well as fears and expectations for the future, into their reasoning when completing the instrument.⁸ It is likely that the meaning attached to problems with breathing and pain for patients with LC early in the disease trajectory may be an important factor influencing their strong association with distress.⁸

Patient and caregiver expectations and affect are argued to influence health outcomes and health care–seeking behaviors.^30-35 These findings raise the question as to whether patients' fears and anxiety about future symptom experiences may therefore be of clinical concern, especially in situations in which better knowledge of and access to palliative care might well diminish unnecessary apprehension and suffering. Although no adequate indicators of apprehension about future symptoms are available in this study, this sample does report high prevalence of disturbances on the emotional function scale, especially on items related to worry and depression. Although different means of assessment were used, Zabora et al⁹ also found LC patients to be at particular risk for psychological distress compared with other cancer patient groups. It is therefore important that efforts be made to minimize negative affect and expectations.

This study was designed to investigate a naturally occurring population receiving a wide variety of treatment modalities and symptom management strategies. This design is therefore not appropriate for systematic assessment of differences in symptomatology by treatment status. On the other hand, treatment-related differences in symptomatology may not be as great in this group as is often assumed. For example Brown et al³⁶ found little evidence of differences in symptoms and functional levels in NSCLC patients with or without chemotherapy. Differences may be minimized as a result of increased use of various palliative cancer treatments. Other limitations should also be considered. Given the salience of dyspnea with regard to its prevalence, intensity, and association with distress in this sample, data not presently available on smoking status and comorbidities such as chronic obstructive pulmonary disease, would have been valuable. It should also be noted that, although this study comprises an unusually large sample in this hard-to-recruit patient group, subsample sizes are still relatively small. Despite limited sample size, we found statistically significant results. Our sample should also be considered in light of the selection bias toward the healthiest of these very sick patients. Participants are younger with longer survival times compared with both nonrespondents and the population of inoperable LC patients in the same region. It should be remembered that these patients represent those with good access to a university hospital specialist department in the capital city of a well-developed country with low direct patient costs for health care. The high prevalence and intensity of somatic and psychological symptoms found in this study thus likely represent an underestimation of these symptoms.

Given this likely underestimation of problems experienced by many other LC patients, these data indicate a strong need for more prophylactic and proactive symptom management for this patient group. Given the high prevalence of symptoms in all subgroups, it is necessary to consider how guidelines for symptom management are to be formulated. Strömgren et al²⁹ argue that it may be more meaningful to evaluate the outcome of a given problem in the subgroup suffering from the problem than in the entire group of patients at an institution. We support this argument, but further emphasize a need to understand suffering as related to individual prioritization of distress, including fears and apprehensions for the future. Future studies should investigate longitudinal associations between symptoms with low intensity and high distress. If low intensity symptoms are strongly associated with distress, one particularly salient issue is how they should be managed clinically. There may be a need for proactive prophylactic management of prevalent symptoms with relatively low intensity, but high association with distress.

	AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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The author(s) indicated no potential conflicts of interest.

	AUTHOR CONTRIBUTIONS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS REFERENCES

 
Conception and design: Carol Tishelman, Lesley F. Degner, Mirjam A.G. Sprangers

Data analysis and interpretation: Carol Tishelman, Lena-Marie Petersson, Mirjam A.G. Sprangers

Manuscript writing: Carol Tishelman, Lena-Marie Petersson, Mirjam A.G. Sprangers

Final approval of manuscript: Carol Tishelman, Lena-Marie Petersson, Lesley F. Degner, Mirjam A.G. Sprangers

	ACKNOWLEDGMENTS

 
We thank Coop Sweden for gift certificates for patients.

	NOTES

 
Supported by the Swedish National Research Council, Swedish Cancer Society, Swedish Heart-Lung Foundation, Swedish Foundation for Health Care Sciences and Allergy Research, and the Center for Health Care Sciences at the Karolinska Institutet.

This study derives from a larger research project with other portions presented in Broberger E, Tishelman C, von Essen L: J Pain Symptom Manage 29:572-583, 2005; Tishelman C, Degner LF, Rudman A, et al: Cancer 104:2013-2021, 2005; Broberger E, Sprangers M, Tishelman, C: Nurs Res 55:274-282, 2006; and Leveälahti H, Tishelman C, Öhlén J: Psycho-oncology 10.1002/pon.1080.

Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.

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Submitted August 17, 2006; accepted August 27, 2007.

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