Death after withdrawal from dialysis: the most common cause of death in a French dialysis population

Béatrice Birmelé1, Maud François1, Josette Pengloan1, Patrick Français2, Didier Testou3, Georges Brillet3, Didier Lechapois4, Serge Baudin5, Olivier Grezard6, Jean-Louis Jourdan7, Mohamed Fodil-Cherif8, Mohamed Abaza9, Luc Dupouet10, Gilles Fournier11 and Hubert Nivet1

1Néphrologie–Immunologie Clinique, CHRU Bretonneau, Tours, 2Centre de dialyse, Clinique Maison Blanche, Vernouillet, 3Centre de Néphrologie, Châteauroux, 4Néphrologie, CHG, Bourges, 5Centre d’hémodialyse, Clinique Saint Côme et Saint Damien, Blois, 6Service de néphrologie, CHR, Orléans, 7Centre d’Hémodialyse de l’Archette, Olivet, 8Clinique d’hémodialyse Jeanne d’Arc, Gien, 9ARAUCO, Tours, 10Service de Néphrologie, CH, Chartres and 11AIRBP, Chartres, France

Correspondence and offprint requests to: Béatrice Birmele, Néphrologie–Immunologie Clinique, CHRU Bretonneau, 2 boulevard Tonnellé, F-37044 Tours, France. Email: b.birmele{at}chu-tours.fr



   Abstract
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 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Background. Discontinuation of dialysis is a common cause of death in end-stage renal disease (ESRD) patients in North America and the UK, but appears to be unusual in the rest of Europe. The aim of this retrospective study was to characterize withdrawal from dialysis in a French population cohort.

Methods. We assessed the cause of death, and the medical and social characteristics of chronic dialysis patients in a French population who died in 2001. We compared patients who died after withdrawal from dialysis and patients continuing dialysis until death. We determined the decision-making process when dialysis was withdrawn.

Results. In a population cohort of 1436 dialysis patients, 196 died (13.9%). Of them, 40 patients (20.4%) died following withdrawal from dialysis. This was the most common cause of death, followed by cardio-vascular disease (18.4%). Patients withdrawing from dialysis had a significantly higher rate of dementia (17.5 vs 6.4%, P = 0.02), a poor general condition (55 vs 15.4%, P < 0.001), and were dependent in their life for everyday activities in comparison with patients who died from other causes. They were not different in age, sex, duration of dialysis treatment, dialysis technique, cardio-vascular disease, diabetes, stroke or cancer, but the sample size was small. Treatment was more often removed in patients with severe medical complications and/or cachexia (90%). The decision to stop dialysis was made most often by a physician (77.5%).

Conclusion. Death after withdrawing from dialysis was the most common cause of death in ESRD patients in our French population cohort. The patients who died after discontinuation of treatment were more often in a poor general condition, near the end of life, and most often the physician decided to stop dialysis treatment.

Keywords: end of life; end-stage renal disease; epidemiology; withdrawal from dialysis



   Introduction
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Withdrawal from dialysis for patients with end-stage renal disease (ESRD) results in death within a few days. It is, therefore, a decision with the most serious consequences. However, the question about continuing such life support treatment must be raised in aging patients with various conditions, including dementia and other mental disorders, which may impair communication and severe cardio-vascular disease. Indeed, in these conditions, what is the aim of continuing dialysis treatment? And if the question is raised, on what basis can such a decision be made? Who is empowered to make the final decision? The patient has the power to stop all medical intervention if he is competent, but if he is not competent, has dementia or is unconscious, who can decide to stop the treatment, their family, the nursing or medical staff, or the nephrologist?

Practices in North America and the UK appear to be different from those in the rest of Europe. Withdrawal from dialysis was a major cause of death in ESRD patients treated by dialysis in the US and Canada. Indeed, for 12–26% of these patients, termination of treatment was the cause of death [17]. However, in Europe, particularly in France, withdrawal from dialysis was the reported cause of only 2–7% of all deaths [4,8,9].

The aim of this study was to assess the condition of patients and the outcome after dialysis withdrawal in a French population cohort (‘Région Centre’). We determined the number of deaths after discontinuation of dialysis and the medical and social conditions of the patients in comparison with patients who died when dialysis sessions were continued until death. We evaluated factors influencing withdrawal from treatment and the decision-making process.



   Subjects and methods
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 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Patient selection
This retrospective study analysed the outcome for all patients with chronic renal failure treated on a chronic dialysis programme for at least during 3 weeks and who died between 01.01.2001 and 31.12.2001 in 11 dialysis units in one area of France, the ‘Region Centre’ (2.5 million inhabitants).

Clinical data
For each patient who died, a questionnaire was completed by the same investigator for all units during an interview with at least one doctor and one nurse of the unit. They used the notes and the medical record of the patient. The cause of death, the date of the last dialysis session and the date of death were examined for each patient who died. Death was considered to be secondary to dialysis withdrawal when the patients lived for >3 days after their last haemodialysis session, or for >7 days after their last peritoneal dialysis procedure [1,10].

The following data were also obtained: age, sex, age at start of dialysis treatment, technique of dialysis (in-centre haemodialysis, self-care unit haemodialysis, ambulatory peritoneal dialysis), the cause of the renal failure, the co-morbid conditions, including diabetes mellitus, severe peripheral vascular disease, severe heart disease, cancer and dementia. We calculated the Davies score, a semi-quantitative co-morbidity scoring [11]. Social and living conditions as well as functional status were considered: where the patient was living (home, rest home or medical institution), family status (living alone, living with spouse or relatives), if the patient was dependent in mobility and for basic activities of daily living (getting up, washing, dressing, eating, ...). We compared the data between two groups of patients: one group with the patients who died after withdrawal from dialysis and one group with the patients who died from other causes and whose dialysis sessions were continued until death.

Clinical notes made by physicians and nurses were carefully reviewed concerning the patients who died after withdrawal from dialysis, particularly the presence and the type of complications when dialysis was stopped and the interval (days) between the last dialysis session and death. Physicians and nurses were questioned about the history of the end of life for these patients. The decision-making process for each patient who died was analysed in each dialysis unit. In particular, we reviewed who initiated the discussion about withdrawal from dialysis, who made the final decision—the patient, his family, the physician or the medical community—and the specific reasons for this decision.

Statistical analysis
Results are expressed as mean±SD for quantitative parameters and percentages for qualitative parameters. Median and range are also presented when the distribution was not Gaussian. Mann–Whitney test was used for the comparison of quantitative parameters. {chi}2 and Fisher's exact test were used for the comparison of percentage as appropriate.



   Results
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 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Death after withdrawal from dialysis
In our population of 1436 patients with chronic renal failure treated by dialysis, 196 (13.9%) died. Of these, 40 patients died following withdrawal from dialysis (20.4% of all patients who died). In all cases, dialysis was terminated despite being technically feasible. The other 156 patients died from other causes (Table 1), and the dialysis sessions were continued until death (79.6% of all patients who died). In the population of patients over 80, the percentage of patients who died after stopping dialysis was 29% (65 patients over 80 died, 19 of them had stopped dialysis). Moreover, withdrawal from dialysis was the first cause of death in dialysis patients in our region.


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Table 1. Causes of death

 
Withdrawal from dialysis as the cause of death was reported in the medical record for 13 patients discontinuing dialysis (6.6% of patients who died). In other cases nothing was reported concerning withdrawal from dialysis or it was only noted that the dialysis session had not been done because of weakness or poor general condition, and so the dialysis session would only prolong this situation and would not be beneficial to the patient. In these cases, it was not reported that the cause of death was withdrawal from dialysis. The causes of death noted were the other medical complications or cachexia.

After the last session of dialysis, the mean survival rate was 8.5±4.8 days (median 7 days, range 4–21 days).

General characteristics of the population
There was no difference in sex between the two groups (Table 2). Patients were almost exclusively Caucasian. The age of the patients in the two groups at the time of death was not significantly different. At the time of death, the mean age of patients stopping dialysis was 77 years (median 79 years, range 46–94), and of patients continuing dialysis until death was 72 years (median 74 years, range 4–101).


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Table 2. Comparison of general characteristics of patients who died after withdrawing from dialysis and patients continuing dialysis until death

 
There was no difference between the two groups in the duration of the dialysis treatment (Table 2), but significantly more patients stopping dialysis had been treated <1 year compared with patients continuing dialysis until death.

There was no difference between the two groups in the type of dialysis technique (haemodialysis or peritoneal dialysis, and in-centre or self-care unit haemodialysis). There was no difference between academic and private dialysis units.

Medical history
There was no difference between the two groups in the aetiology of renal failure (Table 3).


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Table 3. Aetiology of renal failure

 
Co-morbid conditions such as diabetes mellitus, vascular disease, cardiac disease, stroke and cancer were not different in patients discontinuing dialysis and patients who did not discontinue dialysis (Table 4). There was no difference in the Davies score between the two groups. Patients stopping dialysis were more likely to have dementia or poor general condition and cachexia than patients who did not stop treatment. Some patients had no severe medical complications: 30% of patients discontinuing dialysis vs 32% of patients continuing dialysis until death; there was no difference between the two groups.


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Table 4. Medical complications

 
Living conditions and functional status
Two months before death there was no difference between patients discontinuing dialysis and patients continuing dialysis until death, as to the place of life (at home, in a rest home or in a medical institution) or the family status (living alone or with a spouse or with relatives such as children or a sister) (Table 5). In contrast, significantly more patients stopping dialysis were dependent in their life for everyday activities such as getting up, dressing, washing, eating and needing permanent assistance.


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Table 5. Life conditions and functional status

 
At the time of death, 95% of patients for whom dialysis was withdrawn were dependent for everyday activities and 80% were hospitalized.

How was the decision to withdraw dialysis made?
Four patients decided themselves to stop treatment. The physician, the nurses and their family had not suggested this decision. Two of these patients would not continue the treatment because they had become dependent for their everyday activities and needed hospitalization in a medical institution. They chose to withdraw dialysis treatment and subsequently died. One patient had never accepted dialysis treatment despite the fact that he had no medical complications, was not dependent and was not depressive. For the medical team, the patient was competent and able to decide for himself. He stopped 6 months after beginning dialysis treatment. One patient failed to come to his last dialysis session. He was non-compliant and on several occasions had failed to come to the dialysis centre for his treatment.

In all other cases the decision to terminate treatment and withdraw dialysis was made because the general state of the patient had declined: cachexia and weakness in 23 patients, severe peripheral vascular disease in four patients, severe cardiac failure in one patient, dementia in seven patients, pancreatitis in one patient. When the patient was conscious and without dementia, he was invited to participate in the discussion and the decision. In 32 cases, the patient was not able to participate in the decision to withdraw dialysis: seven patients had dementia and 25 patients were not conscious or were too weak. No patient had given advance directives.

In five cases the family initiated the discussion and made the decision about treatment termination, which was accepted by physician and nurses of the dialysis unit. In four cases, the nursing and medical staff of the patient's unit initiated the discussion and decided to withdraw dialysis. In 27 cases, the discussion was initiated by the nursing and medical staff of the dialysis unit: the decision was made with the patient and his family or relatives in four cases, with the family or relatives in 14 cases. In nine cases the decision was made by the nursing and medical staff alone.

The decision-making process in dialysis units
We studied how the decision was made in the 11 dialysis units.

The discussion could always be initiated by the patient or his family and by nurses and physicians of the hospital or rest home where the patient was staying. In the dialysis units, the question of continuing or stopping dialysis treatment for a patient who was weak and in poor general condition could be asked by dialysis physicians in seven units, by nurses in six units, and was never asked in four units.

The decision to terminate treatment could always be made by the patient and/or his family or by the medical staff of the place where the patient was staying. The procedure of such a decision in dialysis units was not the same in all units. In seven dialysis units, the decision was made by the physicians after discussion with the patient and his family when it was possible. In four of these seven dialysis units, the question of stopping treatment was systematically discussed by the nursing and medical staff. The final decision to withdraw dialysis was made by the dialysis physicians. In four dialysis units, the physicians did not make any decision to withdraw dialysis, but accepted to withdraw dialysis when the decision was made by the medical staff of the unit where the patient was staying.



   Discussion
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 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
In our study, 20.4% of patients treated by dialysis died after termination of treatment, 29% in patients aged over 80. This result was similar to the data published in the US and Canada [17,12]. But this percentage was higher than in other European reports [4,8,9], with the exception of a Spanish report in which 26% of patients died after withdrawal from dialysis [13]. The difference between our study and other European studies, except the Spanish study, could be due to differences in dialysis strategies and attitudes of patients and physicians. But these differences could also be induced by the manner of reporting dialysis withdrawal: in our study we defined withdrawal from dialysis taking into account the delay between the last dialysis session and death. So we found that 20.4% of patients died after withdrawal from dialysis, but in only 6.6% of patients who died was termination of treatment reported as the cause of the death in the case notes. Similar results were reported previously [7,14].

At the time of death, the age of patients stopping treatment was not different from the age of patients in which dialysis was not withdrawn. This was found also by Husebye [10], but other studies found that the age of patients who died after termination of treatment was higher than the age of those who died from other causes [2,3,6,15]. However, the percentage of patients withdrawing from dialysis treatment increased in the older population as was shown previously by several authors [5,10,16,17].

The mean time of dialysis treatment was similar in patients of both groups, but significantly more patients who discontinued dialysis died during the first year of the dialysis programme, as also shown previously [5]. This was not surprising: terminal renal failure is only one element of medical complications and of poor general condition in older patients. These multiple medical problems can be present at the beginning of dialysis and can lead to a rapid alteration in physical state and to the decision to terminate treatment.

Patients discontinuing dialysis had no more medical complications than patients continuing dialysis until death. But they were significantly more often in poor general condition and were more likely to have cachexia. In contrast in other studies, patients more often had associated pathologies such as diabetes mellitus, vascular disease, cardiac disease or cancer [1,5,6,1416,18,19]. However, cachexia and poor general conditions were often associated with withdrawal from dialysis in previous studies [5,14,15]. In our study the difference in medical complications (with the exception of cachexia and poor general condition) did not reach the statistical threshold. One could suggest that the sample size was too small. Nevertheless, there was no difference in the Davies score, suggesting that there was effectively no difference between two groups concerning medical complications.

More often, patients withdrawing from dialysis were living at home; only a minority of patients were living in a rest home. Other authors showed that patients withdrawing from dialysis resided more often in medical institutions [3,15]. Patients withdrawing from dialysis were more often invalids than patients who continued dialysis until death. This was also shown previously [6,14,15]. Patients who died after termination of treatment had a very poor quality of life and were near the end of life, the family and medical team were helpless to relieve their suffering. In these cases, the dialysis sessions were discontinued, indeed discontinuation of dialysis seemed to be the most appropriate option.

In most incompetent patients, physicians initiated the termination of dialysis. This was also noted in the early 1970s in the USA, whereas in the 1980s, the family initiated the discussion more often than physicians [1,20]. The physician and/or the nursing staff initiated the discussion and made the decision more often. In contrast, in previous studies, the patient and his family or relatives more often initiated discussion and made decisions [1,2,14,20]. Moreover, when the decision was made in the dialysis unit, it was always the physician who made the decision. A systematic discussion was done among the nursing staff (nurses and aides) in only four units in our study. The discussion did not systematically include a general practitioner, or a multidisciplinary team. The final responsibility for the decision rested with the nephrologist, and it was often desirable that the family did not feel responsible for the decision, since this can lead to feelings of guilt.

This difference could be explained by the fact that in France the idea of taking responsibility for one's own body is less widely accepted than in North America, especially when the outcome may be fatal. Moreover, as demonstrated in our population, the attitude of the physician towards the patient and his family is often a paternalistic one.

In conclusion, death after withdrawing from dialysis was the most common death in dialysis patients in a French population cohort. However, patients who died after discontinuation of treatment were more often in a poor general condition, near the end of life. Therefore, arrest would not be a decision of treatment termination, but rather a non-maleficence attitude, and discontinuation of dialysis appeared to be the most appropriate option. The decision was most often a medical decision, after discussion with the patient, if he was conscious, and with the family. In a few cases, the question of stopping treatment was systematically discussed by the nursing and medical staff.



   Acknowledgments
 
We thank all nephrologists, nurses, aides and secretaries of the dialysis units in the Région Centre for their excellent assistance.

Conflict of interest statement. None declared.



   References
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 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 

  1. Neu S, Kjellstrand CM. Stopping long-term dialysis. An empirical study of withdrawal of life-supporting treatment. N Engl J Med 1986; 314: 14–20[Abstract]
  2. Hirsch DJ. Death from dialysis termination. Nephrol Dial Transplant 1989; 4: 41–44[Abstract]
  3. Bajwa K, Szabo E, Kjellstrand CM. A prospective study of risk factors and decision making in discontinuation of dialysis. Arch Intern Med 1996; 156: 2571–2577[Abstract]
  4. Sehgal AR, Weisheit C, Miura Y, Butzlaff M, Kielstein R, Taguchi Y. Advance directives and withdrawal of dialysis in the United States, Germany, and Japan. JAMA 1996; 276: 1652–1656[Abstract]
  5. Leggat JE, Bloembergen WE, Levine G, Hulbert-Shearon TE, Port FK. An analysis of risk factors for withdrawal from dialysis before death. J Am Soc Nephrol 1997; 8: 1755–1763[Abstract]
  6. Bordenave K, Tzamaloukas AH, Conneen S, Adler K, Keller LK, Murata GH. Twenty-one year mortality in a dialysis unit. Changing effect of withdrawal from dialysis. ASAIO J 1998; 44: 194–198[ISI][Medline]
  7. Holley JL. A single-center review of the death notification form: discontinuing dialysis before death is not a surrogate for withdrawal from dialysis. Am J Kidney Dis 2002; 40: 525–530[CrossRef][ISI][Medline]
  8. Mignon F, Michel C, Viron B, Mentre F, Jaar B. End-stage renal diseases in patients 75 and over: a new medical, socio-economical and ethical challenge. Eur J Med 1992; 1: 302–307[Medline]
  9. Patte D, Wauters JP, Mignon F. Réflexions à propos de l’arrêt des traitements par dialyse. Néphrologie 1994; 15: 7–11[ISI][Medline]
  10. Husebye DG, Kjellstrand CM. Old patients and uremia: rates of acceptance to and withdrawal from dialysis. Int J Artif Organs 1987; 10: 166–172[ISI][Medline]
  11. Davies SJ, Phillips L, Naish PF, Russell GI. Quantifying comorbidity in peritoneal dialysis patients and its relationship to other predictors of survival. Nephrol Dial Transplant 2002; 17: 1085–1092[Abstract/Free Full Text]
  12. Mailloux LU, Belluci AG, Napolitano B, Mossey RT, Wilkes BM, Bluestone PA. Death by withdrawal from dialysis: a 20-year clinical experience. J Am Soc Nephrol 1993; 3: 1631–1637[Abstract]
  13. Rodriguez Jornet A, Garcia Garcia M, Hernando P et al. Patients with end-stage chronic renal insufficiency on programmed withdrawal from dialysis. Nefrologia 2001; 21: 150–159[ISI][Medline]
  14. Catalano C, Goodship THJ, Graham KA et al. Withdrawal of renal replacement therapy in Newcastle upon Tyne: 1964–1993. Nephrol Dial Transplant 1996; 11: 133–139[Abstract]
  15. Sekkarie MA, Moss AH. Withholding and withdrawing dialysis: the role of physician specialty and education and patient functional status. Am J Kidney Dis 1998; 31: 464–472[ISI][Medline]
  16. Port FK, Wolfe RA, Hawthorne VM, Ferguson CW. Discontinuation of dialysis therapy as a cause of death. Am J Nephrol 1989; 9: 145–149[ISI][Medline]
  17. Munshi SK, Vijayakumar N, Taub NA, Bhullar H, Lo TCN, Warwick G. Outcome of renal replacement therapy in the very elderly. Nephrol Dial Transplant 2001; 16: 128–133[Abstract/Free Full Text]
  18. Wenger NS, Lynn J, Oye RK et al. Withholding versus withdrawing life-sustained treatment: patient factors and documentation associated with dialysis decisions. J Am Geriatr Soc 2000; 48: S75–S83[Medline]
  19. Nelson CB, Port FK, Wolfe RA, Guire KE. The association of diabetic status, age, and race to withdrawal from dialysis. J Am Soc Nephrol 1994; 4: 1608–1614[Abstract]
  20. Silva JEM, Kjellstrand CM. Withdrawing life support. Do families and physicians decide as patients do? Nephron 1988; 48: 201–205[ISI][Medline]
Received for publication: 24. 4.03
Accepted in revised form: 10.10.03