Psychological distress and concerns of elderly patients treated with palliative radiotherapy for lung cancer

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1 Psycho-Oncology Psycho-Oncology 16: (2007) Published online 20 November 2006 in Wiley InterScience ( Psychological distress and concerns of elderly patients treated with palliative radiotherapy for lung cancer N. J. Turner 1 *, M. F. Muers 2, R. A. Haward 3 and G. P. Mulley 1 1 Leeds Teaching Hospitals Trust, St James s University Hospital, Beckett Street, Leeds, LS9 7TF, UK 2 Leeds Teaching Hospitals Trust, Leeds General Infirmary, Great George Street, Leeds, LS1 3EX, UK 3 Arthington House, Hospital Lane, Cookridge, Leeds, LS16 6QB, UK * Correspondence to: Leeds Teaching Hospitals Trust, St James s University Hospital, Beckett Street, Leeds, LS9 7TF, UK. Received: 14 April 2006 Accepted: 26 September 2006 Abstract We conducted a prospective observational cohort study of 83 elderly patients (aged 75 and above) being treated with palliative radiotherapy for lung cancer, with a comparison group of 49 younger patients (aged 65 and under). Psychological distress and concerns were measured before and after treatment using the Hospital Anxiety and Depression Scale (HADS) and a Concerns Checklist. Psychosocial morbidity was common, however, prevalence was similar in both age groups. There was a trend towards worsening of both anxiety and depression scores after treatment, but this did not reach statistical significance. Younger patients reported more concerns than the older group (median 12 vs 10) but this too was not statistically significant. Concerns about the illness and symptoms were more likely to have been addressed by the care team than were concerns about psychosocial issues such as the family and the future. People of all ages have similar concerns and levels of anxiety and depression whilst receiving palliative radiotherapy for lung cancer. Further research is needed to explore the use of screening tools, like those used in this study, to identify patients difficulties and target interventions to improve their quality of life. Copyright # 2006 John Wiley & Sons, Ltd. Keywords: cancer; oncology; elderly; quality of life; palliative radiotherapy; anxiety; depression; concerns Introduction Palliative radiotherapy is the commonest treatment for lung cancer. It is used in patients of all ages, though treatment rates decline with increasing age [1]. The median age at diagnosis of patients with lung cancer is currently around 70. Already about 40% of lung cancer patients are aged over 75. Both the median age at diagnosis and proportion of elderly patients are predicted to rise [2]. The management of older patients is therefore a growing problem. The MRC trials on which treatment regimens are based included small proportions of elderly patients [3 5]. Retrospective data suggest that elderly patients benefit from treatment, with improvement in the main symptoms of lung cancer, haemoptysis, chest pain, dyspnoea and cough [6], but there are no prospective studies. Retrospective studies are unable to answer questions about patients quality of life, which is so important in patients receiving palliative treatment. Depression is common in elderly people: it is estimated that around a quarter of elderly inpatients have some depressive symptoms, and of these a quarter to half are severely depressed [7,8]. Similar proportions of cancer patients also have affective disorders [9]. In both patient groups, depression is frequently undiagnosed with studies finding over 50% cases missed in routine practice [10,11]. In addition to having an adverse effect on patients quality of life, depression may worsen prognosis in lung cancer [12]. Data from the three MRC trials found a third of patients treated with palliative radiotherapy to be depressed according to their score on the Hospital Anxiety and Depression Scale (HADS) [13], and this persisted after radiotherapy in more than 50% [14]. There are no data specific to elderly lung cancer patients. Patients anxieties and concerns surrounding their illness affect their quality of life. Concerns including worry about family and the future have been identified in lung cancer patients at diagnosis [15]. Concerns have not been studied at the time of palliative radiotherapy. This study set out to investigate psychological distress and concerns of elderly lung cancer patients treated with palliative radiotherapy. It ran in parallel with a prospective study of Copyright # 2006 John Wiley & Sons, Ltd.

2 708 N. J. Turner et al. effectiveness of treatment in this age group reported elsewhere [16]. Methods A prospective observational cohort study of patients undergoing palliative radiotherapy for lung cancer at a radiotherapy centre was undertaken. All regimens defined as palliative intent by the treating clinician were included. Data were obtained from a group of elderly patients (75 years and above), and from a comparison group of younger patients (aged 65 and under). The only exclusion criteria, apart from age 66 to 74, were severe communication difficulties or dementia (Abbreviated Mental Test (AMT) score [17] of 57/10) such that the patient would be unable to answer quality of life questions even with assistance. The Local Research Ethics Committee approved the protocol and the oncology consultants gave consent to their patients participation. Patients were recruited from radiotherapy planning clinics. A researcher outlined the study, and gave each eligible person a patient information sheet and the opportunity to ask questions. Those agreeing to take part were asked to give written consent to participation and their GPs were informed by letter. Basic demographic details were collected for those who refused consent, and they were invited to give a reason for declining participation. Information on potential confounding variables was recorded. This included demographic data, World Health Organisation (WHO) performance status (PS) [18], a Barthel ADL (activities of daily living) scale [19], disease stage, histology and radiotherapy regimen. Patients completed the HADS (Hospital Anxiety and Depression Scale) [13] and a Concerns Checklist [15] before and after treatment. (They also completed the European Organisation for Research and Treatment of Cancer (EORTC) QLQ- C30 [20] and its companion lung module, LC17, the updated version of the earlier LC13 [21] as part of a broader study examining effectiveness of treatment reported elsewhere.) The HADS was developed for use in people with concurrent physical illness and has been extensively used in cancer patients in particular [22,23]. It was recommended by the MRC working party on quality of life as being particularly useful in cancer patients [24], and was used in the MRC trials in lung cancer [14]. Other studies including elderly patients have also used the HADS successfully [25]. It consists of 14 questions in total, half scoring depressive symptoms and half-assessing degree of anxiety. The Concerns Checklist was developed by the CRC Psychological Medicine Group in Manchester [26] and adapted for use in lung cancer patients in Yorkshire [15]. It has 18 items scored on a fivepoint scale and has been extended to enquire whether concerns have been discussed by the care team. It asks the degree of worry ( not a worry to extremely worried ) about the illness and associated symptoms as well as concerns about family, independence and the future. The first set of questionnaires were completed by patients during their first visit for radiotherapy. Most used touch-screen technology to record their responses. This method has been validated against paper questionnaires [27]. The handheld computer used was a Fujitsu 1600 (# Fujitsu PC Corporation, Santa Clara, CA), with the questionnaires programmed in Microsoft 1 Visual Basic 6 and the data stored in a Microsoft 1 Access version 2 file. For practical purposes, some patients used conventional paper versions: data obtained from the two methods were compared in the analysis. The timing of follow-up was pragmatic, choosing the date of their next outpatient appointment, to minimise travel and to allow patients being seen at peripheral centres to be included. Where possible, Lung Cancer Specialist Nurses in the various peripheral hospitals co-ordinated collection of follow-up data. Where this was not possible, questionnaires along with a reply paid envelope were sent directly to the patients. When no reply was received within 2 weeks, a further set of questionnaires was sent, together with a reminder letter. After this, no further attempts were made to contact non-responders as no reply was taken to indicate withdrawal of participation and a further approach was felt to be unethical. Those returning completed questionnaires were sent a letter of thanks. Statistical methods The anxiety and depression subscales of the HADS were scored using a score of 0 7 ¼ normal, 8 10 ¼ borderline, and ¼ probable case (i.e. likely to have the diagnosis of anxiety or depression confirmed after formal psychiatric assessment). These cut-off scores were recommended by the authors of the scale and have been supported by data from other studies [13,14]. Change over time was determined for each group by comparing caseness before and after treatment. Wilcoxon matched-pairs signed-ranks test [28] was used to test change in scores over time for statistical significance. The concerns checklist data were examined to provide median numbers of concerns identified by each patient group before and after treatment, and the changes over time were compared statistically using Wilcoxon matched-pairs signed-ranks test. The cases reporting major concerns (score 3 4) before treatment were examined to determine the

3 Psychological distress and concerns of elderly patients 709 proportion in whom scores had fallen to minor (score 0 2) after treatment. Median scores for each concern were also calculated before and after treatment. Differences between young and elderly patients were determined on Mann Whitney testing [28]. The proportions of patients who had their concerns addressed by the care team were calculated, with separate analyses for those reporting major and minor concerns. Any differences in proportions of concerns addressed between the two age groups were tested for significance using the w 2 test. All standard statistical techniques were performed using the Statistical Package for the Social Sciences (SPSS) version 9.0 for Windows (# SPSS Inc, Chicago). Results One hundred and ninety one eligible patients were approached over 12 months, of whom 132 (69.1%) were recruited into the study, 83 elderly (75 and over) and 49 younger (65 and under) patients. A further 13 took the first set of questionnaires home but failed to return them and the remaining 46 refused consent. The baseline characteristics of the young and elderly groups are given in Table 1. There were no significant differences between the two groups. The touch-screen was used for initial questionnaire data collection in 55.3% patients, and the proportions were similar in the two age groups. There were no significant differences in median scores between the touch-screen and paper forms of data collection. Follow-up questionnaires were returned by 76 (58%) of the 132 patients entering the study, (42 (51%) elderly and 34 (69%) younger patients). Twenty-nine (52%) of those who did not return follow-up questionnaires died within 3 months of treatment (10 young and 19 elderly). Using the cutoff of a minimum survival of 3 months from treatment to define those from whom follow-up could reasonably be expected, the 76 questionnaires returned represents a compliance rate of 74% (76 of 103 not terminally ill or dead). The median time to follow-up was 57 days (range ) with no difference between the two groups. The proportions of elderly and young patients scoring as borderline or probable cases of anxiety and depression are given in Table 2, both before and after radiotherapy. The proportions were similar in the two groups with a trend for more patients to be depressed at follow-up. Tables 3a d illustrate the changes at the individual level. The number of patients for whom these data were complete was small. This is because a single question left unanswered results in no HADS score. As a result, the totals in the different tables Table 1. Baseline characteristics of study patients Young group Elderly group (n ¼ 49) (n ¼ 83) Age median (range) years 60 (43 65) 78 (75 89) Sex % male WHO performance status (PS) a 0 6% 2% 1 63% 55% 2 31% 39% 3 0% 4% Charlson comorbidity scores Median scores (range) 0 (0 3) 2 (0 5) Carstairs quartiles b 1 24% 25% 2 18% 29% 3 26% 24% 4 32% 22% Disease stage c Early 18% 45% Late 82% 54% Incomplete information 0 1% Histology NSCLC 86% 84% SCLC 12% 8% Clinical diagnosis/unknown 2% 8% Palliative radiotherapy regimen d Low dose 74% 82% High dose 26% 18% a PS 0 ¼ able to carry on normal activity, 1 ¼ able to live at home with tolerable tumour manifestation, 2 ¼ disabling tumour manifestations but 550% time in bed, 3 ¼ severely disabled and 450% time in bed but able to stand. b Measure of socioeconomic status, 1 ¼ most affluent, 4 ¼ least affluent. c All histological types combined, Early ¼ NSCLC stage occult IIB and SCLC limited stage disease, Late ¼ NSCLC stage IIIA IV and SCLC extensive disease. d Low dose ¼ 10 Gy in 1#, 17 Gy in 2# and 20 Gy in 5#; High dose ¼ 36/39 Gy in 12/13#. are not the same, Tables 3a d comprising only those patients who had complete data for each score both before treatment and at follow-up. There were non-significant trends for worsening of both anxiety and depression scores after treatment (Wilcoxon signed-ranks tests: anxiety P ¼ 0:53 young group, P ¼ 0:46 elderly group; depression P ¼ 0:29 young group, P ¼ 0:04 elderly group). The median number of concerns identified by the elderly patients was 10 (range 0 18) before treatment, rising slightly to 10.5 at follow-up. The younger group reported more concerns (median 12, range 0 18 before and after treatment), but the differences between the two groups were not significant (Mann Whitney, P ¼ 0:03 before treatment, P ¼ 0:49 at follow-up). The median scores for each concern are illustrated in Figure 1. Mann Whitney testing revealed no significant differences between scores for

4 710 N. J. Turner et al. Table 2. HADS scores pre- and post-radiotherapy Normal Borderline Case % (n) % (n) % (n) Anxiety: young group Pre-radiotherapy 54 (23/43) 26 (11/43) 21 (9/43) Post-radiotherapy 52 (17/33) 18 (6/33) 30 (10/33) Anxiety: elderly group Pre-radiotherapy 55 (36/65) 32 (21/65) 12 (8/65) Post-radiotherapy 63 (25/40) 13 (5/40) 25 (10/40) Depression: young group Pre-radiotherapy 53 (20/38) 26 (10/38) 21 (8/38) Post-radiotherapy 55 (18/33) 21 (7/33) 24 (8/33) Depression: elderly group Pre-radiotherapy 55 (34/62) 24 (15/62) 21 (13/62) Post-radiotherapy 47 (18/38) 21 (8/38) 32 (12/38) Scores: 0 7 ¼ normal; 8 10 ¼ borderline; ¼ case. Table 3. Change in HADS scores after treatment Pre-radiotherapy anxiety Case Borderline Normal Total (a) Anxiety ratings: young group Post-radiotherapy Anxiety Case Borderline Normal Total (b) Anxiety ratings: elderly group Post-radiotherapy Anxiety Case Borderline Normal Total Pre-radiotherapy depression Case Borderline Normal Total (c) Depression ratings: young group Post-radiotherapy Depression Case Borderline Normal Total (d) Depression ratings: elderly group Post-radiotherapy Depression Case Borderline Normal Total the two age groups. None of the concerns had a median rating of more than 2, i.e. moderately concerned. The young group consistently ranked the illness, the future relating to the illness and family highest. In addition, they rated their energy level as a moderate concern before treatment, but the median score improved to minor at follow-up. The elderly group also ranked family as one of their most serious concerns before treatment, but this improved to mild at follow-up. Breathlessness was consistently rated as a moderate concern by the elderly patients, and their median scores for energy level and future relating to their illness increased from mild to moderate after radiotherapy. The changes in scores over time were analysed for the whole group (age sub-groups were not analysed) using Wilcoxon signed-ranks but none was statistically significant. The proportions of patients reporting major concerns (score 3 4) whose level of concern reduced to minor (score 0 2) at follow-up were calculated (Table 4). As illustrated, the numbers with major concerns were small, so no statistical analyses were done. The proportions within each age group who reported having their concern addressed by the care team are illustrated in Table 5. These data are sub-divided into minor and major concerns. There were high levels of missing data (28% overall) and few patients reported major concerns. Where the total number of patients with a major concern was 510, proportions whose concern had been addressed were not calculated. Because of far greater problems with missing data from follow-up questionnaires (over 80% did not answer some of the has any member of the care team talked to you about this? questions) figures for concerns being addressed after treatment were not calculated. In general, physical symptoms (such as pain and breathlessness) as well as issues about the illness itself and its treatment were more likely to have been addressed than concerns about psychosocial issues (such as family and the future). No significant differences in proportions having concerns addressed were found between the two age groups (w 2 test). Within each age group, differences in proportions of major and minor concerns addressed were analysed (w 2 test); none of the differences was statistically significant. However, in the young group, there were trends for major concerns about the illness to be more frequently addressed than minor concerns (81 vs 41%, P ¼ 0:01). Within the elderly group, similar trends were found for concerns about pain (92 vs 41%, P ¼ 0:001). Discussion Psychosocial morbidity was common, in keeping with previous research [14,29]. However, prevalence was similar in both age groups. The median number of concerns reported was higher than in the work of Hill et al., though the

5 Psychological distress and concerns of elderly patients (Scores: 0 = not a worry, 1 = mildly worried, 2 = moderately worried, 3 = very worried, 4 = extremely worried) 3 Median score Illness Pain Mobility Appetite Energy level Treatment Breathlessness Nausea Future relating to illness Future not relating to illness Independence Emotions Family Cough Feeling a burden Bowels Appearance Other Pre-radiotherapy, young group Pre-radiotherapy, elderly group Post-radiotherapy, young group Post-radiotherapy, elderly group Figure 1. Median concerns scores pre- and post-radiotherapy, by age group Table 4. Major concerns (score 3 4) reducing to minor (score 0 2) after treatment Young group Elderly group % (numbers) % (numbers) Illness 18 (2/11) 46 (6/13) Pain 50 (4/8) 89 (8/9) Mobility 71 (5/7) 33 (2/6) Appetite 73 (8/11) 50 (3/6) Energy 44 (4/9) 33 (2/6) Treatment 75 (3/4) 60 (3/5) Breathlessness 40 (4/10) 43 (3/7) Nausea 100 (4/4) 0 (0/1) Future relating to illness 36 (5/14) 38 (3/8) Future not relating to illness 33 (2/6) 33 (1/3) Independence 33 (1/3) 20 (1/5) Emotions 43 (3/7) 100 (2/2) Family 33 (6/18) 33 (3/9) Cough 71 (5/7) 88 (7/8) Being a burden 69 (9/13) 29 (2/7) Bowels 100 (2/2) 33 (1/3) Appearance 100 (2/2) 50 (1/2) Other 50 (2/4) 100 (2/2) median scores were lower. In common with their findings, older patients reported fewer concerns than younger ones [15]. Also, psychosocial concerns were less likely to have been addressed than concerns about physical symptoms. Apart from some missing data, the HADS did not present any problems, but some patients misinterpreted the concerns checklist. They read the questions about symptoms in particular as asking whether or not they had a symptom, not whether they were worried about it. When this misinterpretation became apparent from their comments, the correct meaning was explained to them. However, this does raise some uncertainty about whether the responses of those who did not comment, or of those completing paper questionnaires at home, were truly about their level of concerns. In common with the findings of Hill Table 5. Concerns addressed: minor concerns (score 0 2) compared with major concerns (score 3 4) (pre-radiotherapy only) % Minor concerns addressed by care team % Major concerns addressed by care team Young Elderly Young Elderly Illness Pain (6/9) n 92 Mobility (1/8) 47 Appetite Energy level Treatment (4/5) 64 Breathlessness Nausea (3/4) (3/4) Future relating to illness Future not relating to illness (2/6) (2/8) Independence (3/5) 54 Emotions (2/9) (2/4) Family Cough (3/8) (5/8) Being a burden Bowels (3/3) (4/5) Appearance (2/3) (0/1) Other (3/5) (2/6) n % not calculated where total number of patients per cell 510, grey figures in brackets represent actual numbers. et al., many patients had difficulty in differentiating the focus of the questions about the future relating/ not relating to their illness [15]. Referring to the care team, when asking whether their concerns had been addressed, was also open to misinterpretation as some did not realise to whom this referred. In its current form, it is likely that this questionnaire would perform better when administered by interview rather than as a self-completion instrument. Missing data items were a problem with papercollected questionnaires. All follow-up questionnaires were collected by this method, so the

6 712 N. J. Turner et al. numbers of complete pre- and post- radiotherapy data were small. Computer touch-screen collection gives complete data and is a very useful method of obtaining patient self-completed questionnaires. It was well received by patients in both age groups. This study confirms that psychosocial morbidity is common. People of all ages have similar concerns and levels of anxiety and depression whilst receiving palliative radiotherapy for lung cancer. More research is needed to determine if routine screening for depression, plus appropriate treatment, would improve quality of life outcomes for these patients. Similarly, further work might include this checklist being used by Lung Cancer Specialist Nurses to try and improve identification of unvoiced concerns. Acknowledgements Grateful thanks to all the radiotherapy planning team at Cookridge Hospital, Leeds for their assistance with the study, in particular Dr M. Bond, Dr M. Snee, Dr D. Bottomley and Dr D. Dodwell. Thanks also to the Lung Cancer Specialist Nurses in Leeds, York, Pontefract, Harrogate, Dewsbury and Bradford Hospitals for help with follow-up. Thanks also to Victoria Allgar for assistance with statistics. The study was funded by the University of Leeds Thoracic Medicine Research Fund. Conflict of interests None. References 1. Northern and Yorkshire Cancer Registry and Information Service Cancer Outcomes Monitoring. Cancer treatment policies and their effects on survival. Key sites study 2: Lung. Leeds, NYCRIS Parsons NR, Somervaille L. Estimation and projection of population lung cancer trends (United Kingdom). Cancer Causes Control 2000;11: MRC LCWP. Inoperable non-small-cell lung cancer (NSCLC): a Medical Research Council randomised trial of palliative radiotherapy with two fractions or ten fractions. Report to the Medical Research Council by its Lung Cancer Working Party. Br J Cancer 1991;63: MRC LCWP. A Medical Research Council (MRC) randomised trial of palliative radiotherapy with two fractions or a single fraction in patients with inoperable non-small-cell lung cancer (NSCLC) and poor performance status. Medical Research Council Lung Cancer Working Party. Br J Cancer 1992;65: MRC LCWP. Randomized trial of palliative twofraction versus more intensive 13-fraction radiotherapy for patients with inoperable non-small cell lung cancer and good performance status. Medical Research Council Lung Cancer Working Party. Clin Oncol 1996;8: Patterson CJ, Hocking M, Bond M, Teale C. Retrospective study of radiotherapy for lung cancer in patients aged 75 years and over. Age Ageing 1998;27: Koenig HG, Meador KG, Cohen HJ, Blazer DG. Depression in elderly hospitalized patients with medical illness. Arch Intern Med 1988;148: O Riordan TG, Hayes JP, Shelley R, O Neill D, Walsh JB, Coakley D. The prevalence of depression in an acute geriatric medical assessment unit. Int J Geriatr Psychiatry 1989;4: Bottomley A. Depression in cancer patients: a literature review. Eur J Cancer Care (Engl) 1998;7: Hardman A, Maguire P, Crowther D. The recognition of psychiatric morbidity on a medical oncology ward. J Psychosom Res 1989;33: Jackson R, Baldwin B. Detecting depression in elderly medically ill patients: the use of the Geriatric Depression Scale compared with medical and nursing observations. Age Ageing 1993;22: Buccheri G. Depressive reactions to lung cancer are common and often followed by a poor outcome. Eur Resp J 1998;11: Zigmond AS, Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr Scand 1983;67: Hopwood P, Stephens RJ. Depression in patients with lung cancer: prevalence and risk factors derived from quality-of-life data. J Clin Oncol 2000;18: Hill KM, Amir Z, Muers MF, Connolly CK, Round CE. Do newly diagnosed lung cancer patients feel their concerns are being met? Eur J Cancer Care (Engl) 2003;12: Turner NJ, Muers MF, Haward RA, Mulley GP. Do elderly people with lung cancer benefit from palliative radiotherapy? Lung Cancer 2005;49: Hodkinson HM. Evaluation of a mental test score for assessment of mental impairment in the elderly. Age Ageing 1972;1: Miller AB, Hoogstraten B, Staquet H, Winkler A. Reporting results of cancer treatment. Cancer 1981;47: Wade DT, Collin C. The Barthel ADL Index: a standard measure of physical disability? Int Disabil Stud 1988;10: Aaronson NK, Ahmedzai S, Bergman B et al. The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology. J Natl Cancer Inst 1993;85: Bergman B, Aaronson NK, Ahmedzai S, Kaasa S, Sullivan M. The EORTC QLQ-LC13: a modular supplement to the EORTC Core Quality of Life Questionnaire (QLQ-C30) for use in lung cancer clinical trials. EORTC Study Group on Quality of Life. Eur J Cancer 1994;30A: Moorey S, Greer S, Watson M et al. The factor structure and factor stability of the hospital anxiety and depression scale in patients with cancer. Br J Psychiatry 1991;158: Maher EJ, Mackenzie C, Young T, Marks D. The use of the Hospital Anxiety and Depression Scale (HADS) and the EORTC QLQ-C30 questionnaires to screen for treatable unmet needs in patients attending routinely for radiotherapy. Cancer Treat Rev 1996;22(Suppl A): Maguire P, Selby P. Assessing quality of life in cancer patients. Br J Cancer 1989;60: Herrmann C. International experiences with the Hospital Anxiety and Depression Scale}a reviewofvalidation data and clinical results. J Psychosom Res 1997; 42: Harrison J, Maguire P, Ibbotson T, MacLeod R, Hopwood P. Concerns, confiding and psychiatric disorder in newly diagnosed cancer patients: a descriptive study. Psychooncology 1994;3:

7 Psychological distress and concerns of elderly patients Velikova G, Wright EP, Smith AB. Automated collection of quality-of-life data: a comparison of paper and computer touch-screen questionnaires. J Clin Oncol 1999;17: Bowers D. Statistics Further from Scratch. Wiley: Chichester, Montazeri A, Milroy R, Hole D, McEwen J, Gillis CR. Anxiety and depression in patients with lung cancer before and after diagnosis: findings from a population in Glasgow, Scotland. J Epidemiol Community Health 1998;52:

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