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a Department of Psychology, University of Alabama, Tuscaloosa, AL
b Applied Gerontology Program, University of Alabama, Tuscaloosa, AL
c Department of Gerontology, University of South Florida, Tampa
d College of Nursing, University of South Florida, Tampa
Correspondence: Rebecca S. Allen, PhD, Department of Psychology and The Applied Gerontology Program, University of Alabama, Box 870348, Tuscaloosa, AL 35487-0348. E-mail: raburge{at}bama.ua.edu.
Decision Editor: Laurence G. Branch, PhD
| Abstract |
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Key Words: Pain Hospice Cognitive impairment Cancer
Book Reviews
Practice Concepts
The Forum
The need to alleviate pain while caring for individuals at the end of life has become a national health concern. From 1992 to 1998, the number of Medicare beneficiaries enrolling in hospice care more than doubled to nearly 360,000 (U.S. General Accounting Office 2000
). The percentage of dying patients receiving hospice care may be close to 40% when the number of deaths nationally is adjusted to reflect only individuals appropriate for hospice (Mahoney 1998
).
Notably, more than 50% of terminal cancer patients have physical suffering that requires sedation in the last days of life (Fainsinger, Miller, Bruera, Hanson, and Maceachern 1991
). However, Kaiser and Brock 1992
found that approximately 20% of elderly decedents with cancer as the cause of death were in moderate to severe pain 6 hours before they died. The treatment of pain is a primary goal of hospice care, and a majority (75%94%) of hospice patients experience pain (Bonneh and Shvartzman 1997
; McCarthy, Addington-Hall, and Altmann 1997
). Being pain-free and having adequate symptom control are integral components of hospice patients' definition of "a good death" (Payne, Hillier, Langley-Evans, and Roberts 1996
). Even high-quality hospice care, however, fails to eliminate pain in up to 75% of cases (McMillan and Tittle 1995
; Zeppetella, O'Doherty, and Collins 2000
). In a study of hospice patients with cancer, pain relief was not optimal, with 42% of patients reporting only one half or less of their pain relieved (McMillan 1996
).
Pain may be expressed as: (a) neuropathic pain pain experienced as numbness or tingling in the nervous system, (b) somatic painpain experienced in the musculoskeletal system, and (c) visceral painpain experienced in the bones of the pelvis, ribs, or sternum. Zeppetella and colleagues (Zeppetella et al. 2000
) found that, among cancer patients admitted to hospice, breakthrough pain was classified as: somatic, 46%; visceral, 30%; neuropathic, 8%; and mixed etiology, 16%. The terminal disease process and some end-of-life medical treatments may intensify affective and physical components of the pain experience, leading to acute exacerbations of pain. Episodic pain, or pain that varies with time, is common among hospice patients with cancer (Swanwick, Haworth, and Lennard 2001
).
Because pain is a subjective experience, including affective and sensory components, the Acute Pain Management Guideline Panel 1992
, Acute Pain Management Guideline Panel 1994
has stated that the single most reliable indicator of acute and postsurgical pain is a person's self-report. The presence of cognitive and sensory deficits, however, may hamper an individual's ability to communicate painful experiences (Farrell, Katz, and Helm 1996
; Horgas and Baltes 1994
; Jancar and Speller 1994
). For example, cognitively impaired nursing home residents are less likely to be identified by health care professionals as suffering from pain (Sengstaken and King 1993
). They are also less likely than their cognitively intact peers to report pain or to receive analgesic medication even when diagnosed with conditions known to be painful, including cancer (Bernabei et al. 1998
; Farrell et al. 1996
; Horgas and Tsai 1998
; Kaasalainen et al. 1998
; Parmelee, Smith, and Katz 1993
; Won et al. 1999
). Weiner and colleagues (Weiner, Peterson, Logue, and Keefe 1998
) found that cognitive impairment was related to lower testretest agreement and greater 4-week variability in intensity of self-reported pain using a 10-point visual analogue scale and a pain thermometer. The authors found that nursing home residents with higher Mini-Mental Status Exam (MMSE; Folstein, Folstein, and McHugh 1975
) scores reported greater pain intensity, and that residents with MMSE scores of 2226 were more likely to show testretest disagreement than residents with MMSE less than 22 or MMSE greater than 26. High scores on the MMSE indicate better cognitive functioning.
Although only 5% of hospice patients have a primary diagnosis of dementia (National Hospice and Palliative Care Organization 2001
), terminally ill individuals are at risk for various types of cognitive impairment. These include not only dementia, but also confusion associated with opioid dosage escalation (Mercadante, Dardanoni, Salvaggio, Armata, and Agnello 1997
), delirium (Lawlor, Fainsinger, and Bruera 2000
), and brain metastases. Martin 1990
found that confusion was common during hospice care, but that neuropsychiatric problems went unrecognized and untreated, and frequently resulted in disturbing, violent, and disruptive patient behavior. Radbruch and colleagues 2000
found that, among older palliative care inpatients, 35% were cognitively impaired using a cut-point of 20 on the MMSE.
Reliance on the self-report of pain as the sole indicator of a hospice patient's pain experience may be further complicated by gender differences in the response to pain and its treatment. There even may be gender differences in the type of pain experienced. Among cancer patients, Mercadante and colleagues (Mercadante, Casuccio, Pumo, and Fulfaro 2000
) found that, in the last 4 weeks of life, visceral pain was more frequently reported among women, whereas men more frequently reported somatic pain. Neuropathic pain was equally reported across gender. Mercadante and colleagues (Mercadante et al. 1997
) found that female gender reduced opioid escalation during the 6 weeks before death. Yeager and colleagues (Yeager, Miaskowski, Dibble, and Wallhagan 1997
) reported that women who were oncology outpatients had more knowledge about pain and pain management. In noncancer research, women typically report higher levels of pain and physical disability, exhibit more pain behaviors, and are more likely to catastrophize in response to the pain experience (Dixon 2001
; Keefe et al. 2000
; Stroud, Thorn, Jensen, and Boothby 2000
; Thorn, Rich, and Boothby 1999
). Coward and Wilkie 2000
, however, found no clear gender differences in pain report among cancer patients with bone metastases. Likewise, Petzke, Radbruch, Zech, Loick, and Grond 1999
found that gender, age, tumor site, stage of cancer, and therapy were not related to the presence of transitory pain.
Given that cognitive functioning and gender differences may affect a person's self-report of pain, caregivers are commonly used as proxies for obtaining pain reports in clinical settings (Fisher et al. 2002
; Krulewitch et al. 2000
; Parmelee 1994
, Parmelee 1996
; Weiner, Peterson, and Keefe 1999
). Hospice staff routinely rely on the report of family caregivers regarding care recipients' symptoms, including pain intensity (Weitzner, Moody, and McMillan 1997
). Yet family caregiver reports of care recipient pain correspond poorly to the patients' self-reported pain experience (Brescia, Portenoy, Ryan, Krasnoff, and Gray 1992
; Gaston-Johansson, Franco, and Zimmerman 1992
). Elliott and colleagues (Elliott, Elliott, Murray, Braun, and Johnson 1996
) found that family caregivers consistently reported greater hospice patient pain and disability than did the patients themselves. Interestingly, cognitive status of the care recipient was associated with caregiver report, but not self-report, of pain in this study. Prior research suggests that the quality of communication among terminally ill individuals, their caregivers, and hospice staff influences patient and caregiver outcomes (Beach 1995
; Hull 1991
). Thus, it is of vital importance to examine the potential impact of care recipients' cognitive impairment and gender on the relation between self-reported and caregiver-reported pain during hospice care.
This study examined the relation of hospice cancer patient self-reported pain, family caregiver report of care recipient pain, discrepancies between care recipient and caregiver pain report, and care recipient cognitive functioning and gender. Our specific hypotheses were as follows. First, we hypothesized that more cognitive errors made by care recipients on a cognitive screening instrument would be associated with lower self-reported pain, but not with care recipient pain as reported by caregivers. Second, we proposed that care recipient cognitive impairment would moderate the relation between self-reported pain and caregiver-reported pain (Farrell et al. 1996
; Parmelee et al. 1993
; Weiner et al. 1998
). We proposed that care recipients with intact cognitive functioning would show higher concordance between their report of pain and their caregivers' report of their pain. Care recipients with evidence of impaired cognitive functioning, however, were predicted to show a lower degree of association between their self-report of pain and the pain report of their family caregivers (Brescia et al. 1992
; Gaston-Johansson et al. 1992
; Weiner et al. 1998
). Furthermore, we predicted that care recipients would consistently report less intense pain than would their caregivers (Elliott et al. 1996
). Our third and final hypothesis was that female care recipients would report more intense pain than male care recipients (Dixon 2001
; Keefe et al. 2000
; Thorn et al. 1999
; Yeager et al. 1997
).
| Methods |
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In 1998, Florida was 1 of the 5 states reporting the highest use of hospice services (29%; U.S. General Accounting Office 2000
). In comparison with national averages, participants in this hospice program have slightly longer lengths of stay (national average = 59 days in 1998; median length of stay 19 days) and a slightly higher tendency to be admitted with a primary cancer diagnosis (national average = 57.4%; U.S. General Accounting Office 2000
).
Participants
Care Recipients
Participants (N = 226) were approached for enrollment in a clinical trial designed to improve the quality of life of cancer patients and their family caregivers receiving hospice care in the home. This trial focuses on symptom management in each of three areas: (a) pain, (b) dyspnea, and (c) constipation. These symptoms are common among terminal cancer patients; care recipients were required to exhibit 2 of the 3 symptoms to be included.
Care recipients were entered into the clinical trial based on the following additional criteria: (a) presence of a diagnosis of terminal cancer, (b) age at least 18 years, (c) presence of a family caregiver, (d) evidence of ability to respond to brief mental status screening on the Short Portable Mental Status Questionnaire (SPMSQ; Pfeiffer 1975
) with a minimum score of six correct responses, (e) ability to give informed consent, (f) at least a sixth-grade education, (g) English-speaking, and (h) Karnofsky Performance Status (KPS; Karnofsky and Burcheral 1949
) score greater than 40 as rated by a home health aide. It is important to note that 23 care recipients were excluded from participation in the clinical trial because of cognitive impairment, defined as a score of 5 or lower on the SPMSQ. A further criterion for inclusion in this study was the presence of pain in the care recipient (N = 191), reported either by the care recipient or the family caregiver at the time of the initial assessment. Finally, 15 (7.9%) persons were lost because of missing or incomplete data. Comparisons between those with or without complete data revealed no significant differences in terms of caregiver age, gender, race, or years of education. Among the care recipient characteristics, no differences were present for age, gender, or years of education. However, care recipients who were eliminated because of missing data had significantly poorer SPMSQ scores in relation to those with complete data (7.66 vs. 9.02, respectively; F(1,189) = 25.10, p < .001). In addition, there were proportionally more White patients among the individuals with complete data, compared with those with missing information (84.6%, 58.3%, respectively;
2 (1) = 5.51, p < .05).
One hundred and seventy-six care recipients met all eligibility criteria and received preintervention assessment. The most frequent cancer diagnoses included lung (33.0%), colon (15.3%), prostate (8.5%), pancreatic (6.3%), and breast (4.5%). The average length of time since diagnosis was 30.30 months (SD = 54.99 months, Range 0360). The average age of care recipients was 70.69 years (SD = 11.34, Range 37.7995.62). Their average level of education was 12.01 years (SD = 3.27, Range 125), and 42.6% were female, 84.7% were White, 7.4% African American, and 6.8% Hispanic (in 1998, 89% of hospice enrollees were White; U.S. General Accounting Office 2000
). Their average score on the SPMSQ was 8.93 correct responses (SD = 0.96, Range 610). Sixty-eight individuals (38.6%) scored between 6 and 8 correct responses on the SPMSQ, indicating impaired cognitive functioning (Erkinjuntti, Sulkava, Wikstrom, and Autio 1987
). Care recipients scoring 9 or greater correct responses on the SPMSQ were considered to have no indication of cognitive impairment. The average KPS score of care recipients was 55.34 (SD = 8.55, Range 40100), and their average activities of daily living index (ADL; Katz, Ford, Moskowitz, Jackson, and Jaffe 1963
) was 4.01 (SD = 3.41, Range 012).
Caregivers
For entry into the study, referred caregivers were required: (a) to not be in active treatment for cancer themselves, (b) to evidence the ability to respond to brief mental status screening on the SPMSQ (Pfeiffer 1975
), with a minimum score of 8 correct responses, (c) to be able to give informed consent, (d) to have at least a sixth-grade education, and (e) to be English-speaking. A higher threshold on the SPMSQ was required for inclusion of caregivers in comparison with care recipients due to the need for caregivers to complete a complex intervention regimen.
One hundred and seventy-six primary caregivers met all eligibility criteria and received preintervention assessment. None of these caregivers had to be excluded based on cognitive impairment, defined as a score of 7 or less on the SPMSQ. Their average age was 63.23 years (SD = 14.06, Range 23.9891.90). Their average level of education was 12.59 years (SD = 2.71, Range 422), 73.9% were female, 85.8% were White, 6.8% were African American, and 6.3% were Hispanic. Their average score on the SPMSQ was 9.64 correct responses (SD = 0.59, Range 810). Sixty-six percent of family caregivers were spouses of the care recipient, 17% were adult children, 17.1% were other relatives.
Design and Procedures
All data used in this study were collected as part of the preintervention phase of the larger study (McMillan 1995
; PI, R01CA77307). A registered nurse and a home health aide with hospice experience were employed by the project to collect assessment information with the care recipient/caregiver dyad in the home. Initial assessment interviews were conducted no more than 48 hr after admission to hospice. A bulleted descriptive overview was given to the caregiver and care recipient, and the project was fully explained prior to obtaining informed consent. The RN then interviewed the caregiver while the home health aide interviewed the care recipient.
Screening and Demographic Measures
SPMSQ (Pfeiffer 1975
)
This simple 10-item test of remote memory, knowledge of current events, and mathematical ability screens for gross cognitive impairment. For purposes of this study, the instrument was scored for the number of correct responses. Erkinjuntti, Sulkava, Wikstrom, and Autio 1987
found that, using a cutoff of eight correct responses and two errors, the sensitivity was 100% and specificity was 89.1% for dementia and 73.2% and 89.1%, respectively, for delirium.
The SPMSQ was originally standardized and validated using adjustments for race and education with community-residing older adults, individuals referred to a multipurpose clinic, and persons residing in congregate living facilities (Pfeiffer 1975
). However, more recent data suggest that it is not necessary to adjust for education in scoring (Erkinjuntti et al. 1987
). Additionally, adjusting scores on other cognitive screening instruments based on race or level of education is controversial and is likely to reduce rather than improve sensitivity and specificity (Ford, Haley, Thrower, West, and Harrell 1996
; Kraemer, Moritz, and Yesavage 1998
). Thus, we do not make scoring adjustments based on education or race in the current study.
KPS (Karnofsky and Burcheral 1949
)
The KPS is a measure of functional status that is widely used in cancer research and oncology settings to assess patient functioning. The KPS is scored on a scale from 0 (dead) to 100 (normal functioning). The KPS has been shown to have moderately high interrater reliability (r = .66.69; Yates, Chalmer, and McKegney 1980
). In the current study, the home health aide who interviewed care recipients assigned the KPS score.
ADL Index (Katz et al. 1963
)
This index assesses six activities involving independence in self-care, including bathing, dressing, toileting, transfer, continence, and feeding. The measure has high interrater reliability, as evidenced by agreement of over 95% between professional raters (Lowenstein and Mogosky 1999
). There is also good evidence for criterion-related and construct validity as indicated by associations with mobility impairment and house confinement following hospital discharge, and significant associations with measures of cognitive and functional abilities (Lowenstein and Mogosky 1999
).
Care Recipient Demographics
Standard demographic data were gathered: age, gender, education level, cancer diagnosis, and length of time since diagnosis.
Caregiver Demographics
Standard demographic data were gathered: age, race, gender, and education.
Outcome Measures
An 11-point numeric rating scale (NRS) was used to assess care recipient pain intensity as reported by the care recipient and the family caregiver at the time of the initial assessment. Participants were asked to respond verbally with a number between 0 (no pain) and 10 (worst pain) to rate pain intensity at that moment (McGuire 1984
; Stewart 1977
). Investigators have found that patients prefer to use the 010 NRS rather than other pain rating scales because the scaling is understandable (Kremer, Atkinson, and Ignelzi 1981
). The NRS correlates well with other measures of pain intensity (r = .59.86; Kremer et al. 1981
) and was found to be a more sensitive predictor than other measures in comparison with a behavioral rating scale for pain (Jensen, Karoly, and Braver 1986
). Discrepancies in pain report were calculated by subtracting the caregiver's report of patient pain from the patient's own self-report of pain. Thus, high positive scores indicate more intense pain reported by the patient, high negative scores indicate more intense pain reported by the caregiver, and scores near zero indicate small discrepancy in the report of pain by patients and caregivers.
| Results |
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The associations among the study variables are reported in Table 1 . More intense self-reports of pain among care recipients were associated with more intense reports of care recipient pain by the family caregiver. Care recipient self-reported pain was also significantly associated with lower SPMSQ score and lower education. Contrary to expectation, better cognitive functioning was associated with self-reports of less intense pain. As shown in Table 1 , the number of years of education of the family caregiver was associated with a number of study variables, including caregiver report of less intense care recipient pain.
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Cognitive Functioning and Discrepancy in Pain Report
Second, we hypothesized that care recipient cognitive impairment would moderate the relation between care recipient self-report of pain and caregiver report of care recipient pain. In comparison with caregivers (M = 4.55, SD = 2.35), care recipients reported experiencing significantly less pain (M = 3.07, SD = 2.82; F(1,175) = 39.36, p < .001). Furthermore, 29.5% of care recipients reported no pain when caregivers reported they had pain; only 3.4% of caregivers reported the care recipient had no pain when he or she reported pain. This discrepancy represents an absolute difference in pain report between care recipients and caregivers, not a difference in magnitude. Greater discrepancy between care recipient and caregiver reports of care recipient pain was significantly associated with lower SPMSQ scores among care recipients (see Table 1 ).
Regression analyses showed that cognitive impairment had a direct effect on self-report of pain when controlling for the effects of care recipient education, t(175) = -2.68, p = .008, standardized beta = -.20, but the model only accounted for 8.4% of the variance, F(2,173) = 7.44, p = .001. However, the quadratic term for the SPMSQ did not account for significant unique variance in self-reported pain after controlling for care recipient education and the linear SPMSQ term. The quadratic SPMSQ term should be significant if the relation between self-reported pain and cognition becomes stronger as cognitive impairment increases. In contrast, the better the care recipient's cognitive functioning, the less intense was the care recipient's self-report of pain.
Self-Report of Pain and Gender
Our third hypothesis was that women with cancer and receiving hospice care would report more intense pain than would men with cancer and receiving hospice care. Examination of the bivariate correlations in Table 1 , however, reveals no significant correlations between gender of the care recipient and their self-report of pain.
| Discussion |
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Our first goal in this study was to examine the relation between care recipient self-report of pain and cognitive functioning. Contrary to research investigating pain self-report among cognitively impaired nursing home residents, we found the care recipients with cognitive impairment in this sample reported more intense pain than their cognitively intact counterparts. Interestingly, Frisoni and colleagues (Frisoni, Fedi, Geroldi, and Trabucchi 1999
) found that symptom report among community-dwelling individuals older than age 75 increased with cognitive impairment. Several possible explanations for this finding exist. First, as disease severity increases, it is possible that cancer patients experience both greater pain and greater cognitive impairment. Second, the cognitive impairment experienced by the cancer patients in this sample could have been relatively mild and may have functioned to release patients' inhibitions about reporting pain experienced in the moment. In contrast, nursing home residents with dementia may have communication deficits, making them less likely to report experiencing pain in the moment. Third, the etiology of cognitive impairment may influence the verbal and behavioral expression of pain. This idea would be interesting to explore in future hospice research, with care recipients suffering from diverse illnesses, including cancer, Alzheimer's disease, vascular dementia, AIDS dementia, and delirium.
As hypothesized, cognitive functioning among care recipients did not impact the pain report of their caregivers. In other words, caregivers of patients with cognitive impairment reported the same amount of care recipient pain as did caregivers of patients without cognitive impairment. It could be that family caregivers rely more heavily on nonverbal behavioral cues to their care recipient's experience of pain. Family caregivers' observation of nonverbal pain behaviors exhibited by their patient may thus provide more accurate, albeit discrepant, pain reports. In a recent study of pain reports by cognitively impaired adults in the community and their caregivers, Krulewitch and colleagues (Krulewitch et al. 2000
) found that the Hospice Approach Discomfort Scale, a tool based on observed pain behaviors, did not correlate well with other measures. Future studies need to further explore the associations between the pain reports of hospice care recipients, their family caregivers, and behavioral indicators of care recipient pain.
Our second goal in this study was to examine the impact of cognitive functioning among care recipients on the relation between care recipient self-report of pain and the family caregiver's report of care recipient pain. Care recipient and family caregiver pain reports were only modestly associated (7.8% shared variance), indicating a high degree of variability in the assessment of care recipient pain. We found that only 3.4% of caregivers reported their care recipient had no pain when the care recipient reported pain, but that more than 29% of care recipients reported no pain when their caregivers reported them to be in pain. Consistent with other studies (Elliott et al. 1996
), we found that cognitive impairment among care recipients was associated with greater discrepancy between the pain reports of care recipients and their family caregivers (i.e., higher pain reports by family caregivers relative to the patient's own self-report of pain).
This finding supports the notion that pain assessment and management during hospice care may be hampered by cognitive impairments in hospice patients. Such discrepancies in pain report may decrease the confidence hospice staff place in a care recipient's self-report, but at this time it is unclear at which level of cognitive impairment the validity of self-report becomes questionable. As in other clinical settings (Fisher et al. 2002
; Krulewitch et al. 2000
; Weiner et al. 1999
), we recommend consideration of proxy pain report by caregivers in conjunction with hospice care recipients' self-report of pain. Such comprehensive assessment will aid in the development of pain treatment programs during hospice care.
Our third goal was to examine gender differences in the pain report of cancer patients receiving hospice care. Previous research has shown that women and men may experience the affective and sensory components of pain differently (Dixon 2001
; Keefe et al. 2000
; Mercadante et al. 1997
; Thorn et al. 1999
). Physiological differences may be partially due to the differential etiology of cancer among men and women. However, women are typically more knowledgeable about pain and symptom management and more emotionally reactive to pain. We found no evidence of gender differences in the report of current pain intensity in this sample.
Several limitations of this study are acknowledged. First, these data were collected as part of a larger intervention study designed to improve symptom management for care recipients and decrease distress among family caregivers of cancer patients receiving hospice care in the home. Thus, exploration of the relation between care recipient cognitive impairment and self-report of pain in relation to family caregiver report of care recipient pain was never intended to be a primary outcome of this study. Indeed, care recipients were excluded on the basis of moderate cognitive impairment (Pfeiffer 1975
).
It is also possible that pain may have been a more salient issue to our participants in comparison with other hospice patients, given that our participants had consented to an intervention focused on symptom management, including pain. Thus, our participants may have reported more intense pain than would the hospice patient population in general. However, pain management was only 1 of 3 target symptoms (i.e., dyspnea, constipation) of this clinical intervention trial, and 75%94% of all hospice patients experience pain (Bonneh and Shvartzman 1997
; McCarthy et al. 1997
). Thus, it is our contention that most hospice patients find pain a very salient issue, with the absence of pain being central to conceptualizations of a good death (Payne et al. 1996
).
In summary, these findings replicate and extend prior research by illuminating the associations between cognitive impairment and pain report during in-home hospice care. Future longitudinal research is needed to examine the impact of care recipient cognitive impairment on self-reported pain and caregiver-reported care recipient pain over time. Such investigations will inform the development of educational interventions in pain management for use by hospice staff with family caregivers.
| Acknowledgments |
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We thank the staff and patients of LifePath Hospice for their assistance. Without their enthusiastic support, this project would not have been possible. Special thanks are extended to Karen Quarles, Adriana Coates, and the staff of the Applied Gerontology Program for assistance in manuscript preparation.
Received for publication June 29, 2001. Accepted for publication December 13, 2001.
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