Individual studies indicate that kidney transplantation is associated with lower mortality and improved quality of life compared with chronic dialysis treatment. We did a systematic review to summarize the benefits of transplantation, aiming to identify characteristics associated with especially large or small relative benefit. Results were not pooled because of expected diversity inherent to observational studies. Risk of bias was assessed using the Downs and Black checklist and items related to time-to-event analysis techniques. MEDLINE and EMBASE were searched up to February 2010. Cohort studies comparing adult chronic dialysis patients with kidney transplantation recipients for clinical outcomes were selected. We identified 110 eligible studies with a total of 1 922 300 participants. Most studies found significantly lower mortality associated with transplantation, and the relative magnitude of the benefit seemed to increase over time (p < 0.001). Most studies also found that the risk of cardiovascular events was significantly reduced among transplant recipients. Quality of life was significantly and substantially better among transplant recipients. Despite increases in the age and comorbidity of contemporary transplant recipients, the relative benefits of transplantation seem to be increasing over time. These findings validate current attempts to increase the number of people worldwide that benefit from kidney transplantation.

Abbreviations:

ESRD: end-stage renal disease
EQ-5D: European quality of life-5 dimensions
GHQ: general health questionnaire
HR: hazard ratio
HUI: health utility index
KDQoL: kidney disease quality of life
QoL: quality of life
SES: socio-economic status
SF-36: Medical Outcomes Study 36-item short-form health survey
SIP: sickness impact profile
TTO: time trade off
WHO-QoL: World Health Organization quality of life
15D: Finnish 15 dimensions

Introduction

Available treatments for end-stage renal disease (ESRD) include dialysis and kidney transplantation (1,2). Increasing prevalence of ESRD, together with stable or declining rates of organ donation have led to a critical shortage of kidneys available for transplantation (3,4). The median interval between placement on a transplant waiting list and receipt of a kidney transplant from a deceased donor has dramatically increased in recent years, and currently ranges between 3 and 7 years for North American patients with kidney failure, depending on region of residence (5). At the same time, the age and comorbidity of patients who are treated with dialysis continues to increase (6).

Individual studies indicate that kidney transplantation is associated with lower mortality and improved quality of life compared with chronic dialysis treatment (7,8). However, factors that are associated with greater or lesser benefit from transplantation are poorly described. In addition, there has been little or no systematic exploration of how the relative benefits of transplantation (compared to dialysis) have varied over time, given that contemporary dialysis patients are older and sicker (6), but must wait longer to receive a kidney transplant than those in previous years (3,9).

We did a systematic review to summarize the anticipated clinical benefit associated with kidney transplantation (compared with dialysis) in the current era. We also aimed to identify characteristics associated with especially large or small relative benefit, compared to dialysis.

Materials and Methods

Data sources and searches

This systematic review is reported according to published guidelines (10). An expert librarian conducted a comprehensive search to identify all relevant studies regardless of publication status. Nonenglish articles were included where an appropriate translator was available. Three electronic databases, MEDLINE (1950–February 25, 2010), EMBASE (1980–February 25, 2010), and all evidence-based medicine reviews (September 7, 2007) were searched. The detailed search strategies are included in the Supporting Information. A content expert and a methodologist screened each citation or abstract. Any study considered potentially relevant by at least one reviewer was recovered for further review.

Study selection

The full text of each potentially relevant study was independently assessed by two reviewers for inclusion in the review using predetermined eligibility criteria on a preprinted form. Studies were eligible for inclusion if they reported important clinical outcomes (mortality, cardiovascular events, hospitalization and quality of life [QoL]) in both a chronic dialysis population and a kidney transplantation population. Pediatric studies (age < 16 years) and studies including multi-organ transplantation were excluded. Studies had to include at least 30 participants in each relevant treatment modality group. This minimum sample size was set to improve the efficiency of the work without an appreciable loss of power and to minimize bias (robust calculations of standard deviation and to prevent small study bias). Multigroup cohort studies were included; crossover, case-control and cross-sectional studies were excluded with one exception—we included cross-sectional studies when QoL was reported. Disagreements were resolved by discussion and consultation with a third party. Reviewers agreed on study selection for 89% of the articles (κ= 0.66).

Data extraction and risk of bias assessment

We assessed and reported risk of bias in included studies using items from the Downs and Black checklist (11). These include items of study design (selection of participants, allocation of participants and outcome definitions), statistical analysis (calculation of sample size and adjustment for potential confounding) and results (losses to follow up). Post hoc, we included three items specifically relevant to the time-to-event analyses in these studies: (1) selected time of origin (e.g. dialysis initiation or transplantation) and destination (e.g. modality failure, death), (2) adjustment for prior time spent on renal replacement therapy and (3) modeling time-dependency of modality (i.e. attributing the time on dialysis for eventual transplant recipients and graft failure patients to the dialysis hazard). Two reviewers independently assessed each included study, and resolved disagreements with the aid of a third party.

The following properties were extracted from each study: characteristics (country, data source, era of accrual, duration of follow-up, special subgroups or populations, sample size and setting), participants (age, gender, race, body mass index, socio-economic status and comorbidities), renal replacement modality (living or deceased donor, hemodialysis, peritoneal dialysis, etc.) and results (both unadjusted and adjusted, covariates, interactions and subgroups). The following outcomes were considered: all-cause mortality, cardiac events (limited to myocardial infarction, stroke, heart failure and to the aggregate of any cardiac event), hospitalization (incidence, rate, mean counts; limited to infection and all-cause) and QoL. Specifically, the following QoL instruments were included: European quality of life-5 dimensions (EQ-5D), time trade off (TTO), standard gamble, health utility index (HUI), Finnish 15 dimensions (15D), Medical Outcomes Study 36-Item Short-Form Health Survey (SF-36), kidney disease quality of life (KDQoL), Karnofsky, sickness impact profile (SIP), general health questionnaire (GHQ), and World Health Organization quality of life (WHO-QoL). A second reviewer checked the data for accuracy.

Data synthesis and analysis

Because identified studies were expected to be observational and, therefore, both methodologically and clinically diverse, we decided a priori not to statistically combine results. To facilitate comparison, we present individual study summary statistics in unpooled metagraphs using R software. Dichotomous outcomes (e.g. mortality) are summarized using the unadjusted risk ratio and all available adjusted ratios (i.e. hazard ratio [HR], risk ratio, odds ratio, rate ratio; depending on what was reported). Continuous outcomes (e.g. QoL) are summarized using the mean difference. Given the presence of large heterogeneity, we did not formally assess for the presence of publication bias (12).

We planned a priori to examine the following subgroups for evidence of effect modification on the association between transplantation and mortality: diabetic patients, elderly patients, patients with chronic infections (human immunodeficiency virus, hepatitis B or hepatitis C) and patients with cardiovascular disease. We were primarily interested in the results of formal tests for effect modification in the primary studies. Unfortunately, we did not identify eligible studies for all of these subgroups. However, using multivariable meta-regression models (weighted least squares linear regression), we examined whether era (midyear of the interval for inclusion of participants), restricting analyses to dialysis patients who were active on the kidney transplantation waiting list, or elements of study design (prospective, retrospective or registry) modified the relationship between unadjusted mortality and modality. To minimize participant overlap (and ensure independence of data) between studies in our meta-regression analyses, we restricted our pool of studies to unique combinations of region (or registry) and era of accrual. More current studies were given precedence; studies with special populations were excluded (e.g. hepatitis positive).

Results

Search yield

From 32 166 identified citations, 732 articles were recovered for detailed evaluation (Figure 1). Of these, 110 studies were eligible for inclusion in this review (Table 1). Study sample sizes ranged from 39 to 468 681 (median 501); enrolment of study participants ranged from 1960 to 2006 and maximum duration of follow up ranged from 6 months to 19 years.

Details are in the caption following the image — **Figure 1**
Open in figure viewer PowerPoint

**PRISMA flow diagram.** PRISMA = preferred reporting items for systematic reviews and meta-analyses); ESRD = end-stage renal disease. Details of the search strategies including data sources are in the Supporting Information.

Table 1. Clinical and demographic characteristics of included studies

Author and year	Country	Source	Accrual era	Maximum follow-up (years)	Population	Treatment	Sample size	Mean age (years)	Percent male	Percent diabetic
Bayat (43) 2010	France	Regional registry	1997–2003	7	60–80 years	Tx/D	54/940	63	57	41
Bayat (43) 2010					<60 years		280/221		62	21
Ansell (96) 2009	UK	UKRR	1997–2006	1	−	Tx/D	17,545/22, 115	−	−	−
Buturovic-Ponikvar (65) 2009	Slovenia	ERA-EDTA	1998–2006	9	−	Tx/HD; PD	461/1271; 103	52/65; 53²	57/55; 59	14/24; 21
Chauveau (27) 2009	France	−	1985–2000	11¹	Low protein diet	Tx/HD	101/102	42/62	52/-	−
Griva (88) 2009	UK	Two sites	−	None⁶	−	Tx/HD; PD	117/77; 68	50/50	60/65	5/17
Jain (37) 2009	UK	Multiple sites	1996–2000	4²	White; Black; South Asian	Tx/HD; PD	157/598	62²	63	25
Kramer (70) 2009	Europe	ERA-EDTA	1997–2006	10	−	CTx; LTx/HD; PD	20, 321; 2965/398, 871; 46, 524	46/63	63/61	12/22
Martin Navarro (16) 2009	Spain	−	2000–2005	2²	WL; nWL; ECD	CTx/WL HD	31/164	68/74	64	35/20
Pauly (59) 2009	Canada; USA	USRDS; Regional registry	1994–2006	4²	−	CTx; LTx/Night	531; 531/177	47; 44/46	58; 57/65	14; 14/14⁴
Stel (97) 2009	Europe	ERA-EDTA	2000–2004	2	−	CTx; LTx/HD; PD	13,753; 3505/7,137	−	−	−
Patel (98) 2008	UK	Single site	2002–2005	3²	−	CTx/WL HD; PD [nWL HD; PD]	80/142 [78]	51 [54]	64	19 [39]
Visnja (14) 2008	Serbia	Single site	1987–2001	17	HBV+;	Tx/WL HD	67/128	35/50	75/58	0/8⁴
					HCV+;		39/83	36/55	69/48	5/8
					Hep–		278/192	33/50	68/53	2/5
Chavers (52) 2007	USA	USRDS	1996–2001	3	−	Tx/HD; PD	31,663/333,453	<65/65–74²	60/53	29/45⁴
Gill (77) 2007	USA	USRDS	1995–2003	−	−	CTx; LTx[GF]/WL D	47,433 [5,461]/41,	49 [48]/50	62 [61]/60	30 [25]/36⁴ 769
Sorenson (30) 2007	Denmark	ERA-EDTA; Multi-national registry	1994–2005	7¹	DM; nDM	Tx/WL HD; PD [WL HD; PD]	1,239/517 [4,737]	41/49 [66]	−	17/22 [24]
Cheawchanwattana (81) 2006	Thailand	Single site	2005	None	−	Tx/HD; PD	133/107; 62	45/45; 57	65/60; 55	23/18; 47
Snyder (31) 2006	USA	USRDS	1995–2003	−	DM;	Tx/WL D	11,418/19,107	50–64²	60/59	100
Snyder (31) 2006					nDM		32,009/34,202	35–49	60/59	0
Yildirim (92) 2006	Turkey	Multiple sites	2004–2005	None	−	Tx/HD; PD	356/104; 186	44/55; 46	56/46; 53	−
Zimmerman (55) 2006	Brazil	Single site	1996–1997	None³	−	Tx/HD	64/40	45	55	−
Borentain (25) 2005	France	Single site	1995–2001	4	PTCA	Tx/D	37/75	52/61	95/69	11/32
Buturovic-Ponikvar (99) 2005	Slovenia	Multiple sites	2003	1	−	Tx/HD; PD	374/1171; 116	−	−	−/19
Ho (68) 2005	China	Regional registry	1995–2004	7	−	Tx/HD; PD	3,174/1,119; 5,149	49–55²	∼59/52; 49	12/23; 39
Lee (83) 2005	Wales	Single site	2002	None	−	Tx/HD; PD	209/99; 74	53/63; 59	60/61; 51	−
Massad (26) 2005	USA	Single site	1992–2004	−	CABG	Tx/HD; PD	32/62	58/58	59/63	50/76
Merion (17) 2005	USA	National registry	1995–2002	10	ECD;	CTx; LTx/D	7,790 [41,052];	40–59 [40–59]; −/40–59²	62 [61]; −/58	27 [22]; −/35⁴
Merion (17) 2005					nECD		15,203/45,082
Niu (100) 2005	Taiwan	Two sites	2002	None	−	Tx/HD; PD	80/80; 80	43/55; 51	44/40; 43	−
Oniscu (49) 2005	UK	Multiple regional registries	1989–1999	3	−	CTx/WL HD; PD	1,095/641	43/53	61/62	12/19⁴
Schaubel (101) 2005	USA	National registry	1999	3	−	CTx; LTx/D	7,773/8,011	−	−	−
Abbott (15) 2004	USA	USRDS	1995–2000	6	HCV+donor; HCV–donor	CAD/WL D	389; 16,495/17,044	51; 46/50	75; 63/60	30; 34/40⁴
Moe (102) 2004	USA	Single site	−	2	−	Tx/HD	38/30	45/55	76/61	37/94
Oniscu (46) 2004	UK	Multiple regional registries	1989–1999	11	≥60 years	Tx/HD; PD	128/197	64/66	65/59	13/16
Schon (103) 2004	Sweden	National registry	1991–2002	12	−	CTx; LTx/HD; PD	721/3,052; 1,294	−	−	17/33; 35
Sezer (13) 2004	Turkey	Single site	<1996	5	nDM: HCV+ HCV–	CTx; LTx/HD CTx; LTx/HD	116/136	34/43	71/60	0
Abbott (104) 2003	USA	USRDS	1994–1997	−	−	Tx/HD; PD	19,033/16,182	43/47	61/58	31/36⁴
Brunkhorst (19) 2003	Germany	Regional registry	1978–1996	19	ESRD-DM; DM1	DM1; DN	46/46	43/45	69/69	100
Glanton (35) 2003	USA	USRDS	1995–1999	7	Obese	CTx; LTx/HD; PD	1,719; 552/5,172	48	54	40
Glanton (35) 2003					nObese	CTx; LTx/HD; PD	4,795; 1,528/16,896
McDonald (40) 2003	Australia; New Zealand	ANZDATA	1991–2000	9	nIndigenous; ATSI;	Tx/HD; PD	12,984	60²	59	17⁴
					Pacific;		1,061	48	43	47
					Maori		502	51	48	55
							935	44	57	63
Tomasz (105) 2003	Poland	Two sites	−	None	−	Tx/HD	83/61	43/58	52/56	−
Baiardi (80) 2002	Italy	Single site	1997–1999	None³	−	Tx/HD; PD	34/171; 30	44/62; 64	65/63; 63	3/6; 7
McDonald (48) 2002 A	Australia; New Zealand	ANZDATA	1991–2001	10	−	CTx/WL HD; PD [nWL HD; PD]	2,362/2,782 [5,052]	44/46 [53]	63/58 [53]	89/75 [50]
McDonald (106) 2002 B	Australia; New Zealand	ANZDATA	2000	1	Australia; New Zealand	Tx/HD; PD	1,764 417	−	−	−
Piccoli (107) 2002	Italy	Regional registry	1995–1999	None	nDM	Tx;GF/HD; PD	92; 40/56	51; 52/60	59; 73/54	0
Abbott (18) 2001	USA	USRDS	1994–1997	2¹	ESRD-DM	Tx/HD; PD	5,683/5,686	47	60	100
Bakewell (39) 2001	UK	Single site	1998	None	South Asian; White	Tx/HD; PD	40/40; 40	46/53; 49	70/65; 70	10/30; 30
Rebollo (45) 2001	Spain	Multiple sites	−	None	<65 years	Tx/HD	213/116	49/56	66/58	7/10
Schmidt (24) 2001	Austria	Single site	1994–1998	5	PTCA	Tx/HD	42/42	59/57	81/76	17/26
Staathof-Galema (79) 2001	Netherlands	Two sites	1990–1996	7	−	CTx; LTx/HD	54/102	50/48	61/63	3/3
Choi (32) 2000	South Korea	Single site	−	0.5	DM; nDM	Tx/PD	71/101	59/58	−	30/18
Fujisawa (82) 2000	Japan	Two sites	−	None	−	CTx; LTx/WL HD [nWL HD]	117/49 [65]	44/46 [46]	43/76 [69]	4/4[5]
Johnson (44) 2000	Australia	Single site	1993–1997	6	>60 years	CTx/D	67/107	66/66	49/41	8/20
Rabbat (50) 2000	Canada	CORR	1990–1994	6	−	CTx/D	722/1,156	44	63/62	18/22⁴
Rebollo (86) 2000	Spain	Multiple sites	1996	None	−	CTx/HD	210/170	51/67	67/51	7/12⁴
Ward (20) 2000	USA	USRDS	1987–1994	3²	Females: ESRD-Lupus	Tx/D	946/3,431	36/40	0	−
					ESRD		5,173/66,202	41/61		100⁴
					ESRD		12,733/100,980	43/62		−
Mazzuchi (53) 1999	Uruguay	Multiple sites	1981–1998	10	−	Tx/HD	460/695	37/60	67/63	7/17
Wolfe (62) 1999	USA	USRDS	1991–1996	7	−	CTx/D	23,275/22,889	40–59/40–59²	63/58	31/35⁴
Lim (73) 1998	Malaysia	National registry	1992–1995	4	−	Tx/HD[Home]; PD	909/1,260; 307	34/42; 46	57/66; 54	9/26; 34
Schnuelle (8) 1998	Germany	Regional registry	1989–1997	8	−	Tx/HD	144/167	48/44	60/62	5/14
Segoloni (78) 1998	Italy	Single site	1992–1996	5	−	Tx/WL D	344/916	45/46	60/64	1/2⁴
Spencer (41) 1998	Australia	−	1978–1996	18	Indigenous; nIndigenous	Tx/D	56/158	45	46	41
Wight (87) 1998	UK	Single site	1995	None	−	Tx/HD; PD; Home; Sat	228/100; 109; 42; 41	40–49/50–59; 50–59; 40–49; 60–69²	62/56; 57; 69; 59	10/11; 22; 0; 20⁴
Bonal (56) 1997	Spain	Regional registry	1984–1993	10	−	CTx/HD	157/395	62/61	58/62	0⁴
Lui (108) 1997	China	Regional registry	1995–1996	1	−	CTx; LTx/HD; PD	957/495; 1,885	41/48; 57	57/52; 50	6/11; 24
Ozminkowski (85) 1997	USA	National registry	1992–1995	None	−	Tx/D	211/304	45–59²	54	29⁴
Boni (63) 1996	Brazil	Single site	−	3	−	CTx; LTx/HD; PD	36/36	33/33	67/61	3/3⁴
Agodoa (109) 1995	USA	USRDS	1980–1990	−	−	CTx; LTx/HD; Home; Self; PD	9,065/121,987	60–64²	62²	30
Disney (66) 1995	Australia	ANZDATA	1983–1992	3	−	Tx/HD; PD	4,381/6,635	−/45–64²	−/54–60²	8–26⁴
Locatelli (61) 1995	Italy	Regional registry	1983–1992	−	−	Tx/HD; PD	1,450/6,823	57	58	3–7⁴
Schaubel (54) 1995	Canada	CORR	1987–1993	7	−	Tx/D	284/6,116	60–69/60–69²	66/58	12/22
Teraoka (110) 1995	Japan	Multiple society registries	1964–2002	9	−	CTx; LTx/HD; Home; Night; PD	6,367/123,926	−	−	−
Cowie (21) 1994	USA	Regional registry	1974–1983	9	<65 years:	Tx/D	129/117	35	62	100
					ESRD-DM1;		50/298	55	49	100
					ESRD-DM2
El-Reshaid (111) 1994	Kuwait	Multiple sites	1986–1990	5	−	CTx; LTx/HD; PD	289/358	45²	64	15⁴
Ojo (38) 1994	USA	Multiple regional registries	1984–1989	6	Black	CTx/D	236/554	40/40	66/66	25/24
Pugh (42) 1994	USA	Regional registry	1975–1985	−	nHispanic White;	Tx/HD; Home; PD	649/4,731	50–59²	−	22⁴
					Mexican-Amercian;		264/2,898	50–59		44
					Black		261/3,160	50–59		20
Del Pilar Garofano Plazas (112) 1993	Spain	Multiple sites	−	None	−	Tx/HD	45/111	38/54	56/50	0/7⁴
Port (7) 1993	USA	Multiple regional registries	1984–1989	6	<65 years	CTx/WL D [nWL D]	799/770 [3,451]	−	60 [−]
Brunori (113) 1992	Italy	Single site	1981–1990	10	−	CTx/HD; PD	228/188; 232	36/53	−	−
Alamartine (57) 1991	France	Single site	1973–1987	15	−	Tx/D	120/158	45	38/51	−
Julius (114) 1989	USA	Regional registry	1981–1984	None	−	CTx; LTx/HD; PD	83; 80/171; 125	41–60; 20–40/41–60; 41–60²	52; 61/49; 54	25; 34/26; 17⁴
Kjellstrand (115) 1989	USA	Two sites	1963–1985	−	−	Tx/D	2,579/2,004	−	−	−
Petrie (116) 1989	New Zealand	Single site	−	None	−	CTx/HD; PD	30/75	39/43	67/55	−.
Silins (75) 1989	Canada	National registry	1981–1986	5	−	Tx/D	2,436/5,996	45–64²	61	18⁴
Fauchald (67) 1988	Norway	Multiple sites	1981–1985	6	−	CTx; LTx/WL D [nWL D]	122/127 [119]	66/66 [70]	69	−
Morris (117) 1988	UK	Single site	−	None	−	Tx/HD; Home; PD	69/69	49/54	40/34	−
Burton (51) 1987	UK	Single site	1974–1985	11	−	CTx; LTx/HD; PD	183/276; 158	38/42; 51	64/63; 58	5/4; 12⁴
Churchill (118) 1987	Canada	Single site	−	None³	−	Tx/HD; Home; PD	79/42; 42; 31	−	−	−
Khauli (22) 1986	USA	Single site	1976–1982	8	ESRD-DM; DM1	CTx; LTx/D	52/48	34/41	−	100
Khauli (33) 1986⁵	USA	Single site	1976–1982	8	DM	CTx; LTx/HD; PD	48/52	33/42	−	100
Evans (119) 1985	USA	Multiple sites	−	None	−	CTx; LTx/HD; Home; PD	144/347; 287; 81	37/52; 47; 50	48/50; 64; 46	8/10; 8; 16
Garcia-Garcia (58) 1985	USA	Single site	1973–1981	9	−	CTx; LTx/D	103/238	47	45	28/29
Minetti (120) 1985	Italy	−	1972–1985	14	−	CTx/HD WL	284/211	−	−	−
Hellerstedt (121) 1984	USA	Multiple sites	1978–1983	6	−	CTx; LTx/HD; Home; PD	1,187/1,999	21–45/46–60²	62/55	−
Zimmerman (34) 1984	USA	Two sites	1971–1983	−	DM	CTx; LTx/HD; PD	36; 37/66	37; 31/48	−	100
Krakauer (69) 1983	USA	National registry	1977–1980	−	−	CTx; LTx/D	7,595; 3,491/65,270	31–40; 21–30/>50²	63; 60/56	7; 8/9⁴
Kramer (23) 1983	Europe	EDTA-ERA	1976–1981	−	ESRD-Lupus;	Tx; GF/D	120; 48/815	−	−	−
Kramer (23) 1983					ESRD-PCKD		1,085; 407/6,293
Vollmer (60) 1983	USA	Multiple sites	1960–1979	19	−	CTx; LTx/D	255/594	45–54²	55	11⁴
Cestero (122) 1980	USA	Multiple sites	1967–1978	−	−	Tx/HD; Home	150/299; 109	43–48	−	−
Nicholls (123) 1980	UK	−	1968–1978	10	−	CTx/D	48/50	37	−	−
Avram (124) 1979	USA	Single site	1973–1978	5	−	CTx; LTx/DM D [nDM D]	69/122 [482]	−	75/63 [57]	6/100 [0]
Dumler (125) 1979	USA	Single site	1972–1978	6	−	CTx: LTx/HD	140/443	40/62	−	0
Hull (126) 1979	USA	Single site	≥1970	5	−	CTx; LTx/D	248/605	−	56	−
Bonney (127) 1978	USA	Multiple sites	1967–1975	8	−	CTx/HD; Home	84/328; 41	30/43; 46	−	0/30; 2⁴
Golper (128) 1978	USA	Single site	1971–1977	7	>45 years	CTx/D	30/51	51/51	−	3
Kreis (71) 1978	France	Single site	1962–1976	7	−	CTx/HD; Home	272/440; 210	30/<50	−	−
Price (74) 1978	Canada	Single site	1964–1976	12	−	CTx/HD; Home; PD	305	38	67	−
Cantaluppi (76) 1977	Italy	Single site	≥1972	5	−	CTx; LTx/HD; Home	66/61	34/37	71/66	−
Higgins (129) 1977	Canada	Single site	1962–1975	−	−	Tx/HD	87/55	31	62	2⁴
Rao (29) 1977	USA	Single site	1972–1976	5	DM	CTx; LTx/HD	160/60	35/40	64/57	100
Bonomini (64) 1975	Italy	Single site	1966–1974	9	−	CTx; LTx/D	39/113	−	−	−
Krumlovsky (72) 1975	USA	Single site	1970–1974	5	−	CTx; LTx/HD	85/92	−	−	−
Lowrie (130) 1973	USA	−	1964–1972	9	−	CTx; LPTx; LSTx/Home	112; 93; 79/125	38; 24; 36/44	62; 71; 58/73	1; 1; 0/5⁴

USA = United States of America; GOV = government; UK = United Kingdom; UKRR = United Kingdom Renal Registry; ERA-EDTA = European Renal Association-European Dialysis and Transplant Association; USRDS = United States Renal Data System; ANZDATA = Australia and New Zealand Dialysis and Transplant Registry; CORR = Canadian Organ Replacement Register; WL = waitlisted; nWL = not waitlisted; ECD = extended-criteria donor; HBV+= hepatitus B virus positive; HCV+= hepatitis C virus positive; Hep–= hepatitis negative; DM = diabetes mellitus; nDM = no diabetes mellitus; PTCA = percutaneous transluminal coronary angioplasty; CABG = coronary artery bypass graft; nECD = not expanded criteria donor; HCV+ donor = hepatitis C virus donor; HCV– donor = hepatitis C virus negative donor; HCV–= hepatitus C virus negative; ESRD-DM = end-stage renal disease caused by diabetes mellitus; DM1 = diabetes mellitus type 1; nObese = not obese; nIndigenous = non-indigenous; ATSI = aboriginal and Torres strait islander; ESRD-Lupus end-stage renal disease caused by lupus; ESRD-Other = end-stage renal disease caused by something other than diabetes mellitus or lupus; ESRD-DM2 = end-stage renal disease caused by diabetes mellitus type 2; nHispanic = non-Hispanic; ESRD-PCKD = end-stage renal disease caused by polycystic kidney disease; CTx = cadaveric donor transplantation; LTx = living donor transplantation; HD = hemodiaylsis; PD = peritoneal dialysis; Tx = trasnplantation; GF = graft failure dialysis; Home = home hemodialysis; Self = self hemodialysis; Sat = dialysis at a satellite unit; Night = nocturnal hemodialysis; D = dialysis; LPTx = living parent donor transplantation; LSTx = living sibling donor transplantation. The studies are sorted by year and the first author's last name.
¹Mean.
²Median.
³There was a second interview.
⁴Cause of end-stage renal disease.
⁵This study used the same transplantation group as the other Khauli 1986 study.
⁶Quality-of-life studies were not excluded if they had cross-sectional designs.

Populations studied

Dialysis modalities considered in eligible studies included in-center hemodialysis, satellite hemodialysis, home hemodialysis, nocturnal dialysis, peritoneal dialysis and multiple modalities (populations including both hemodialysis and peritoneal dialysis). Transplantation used allografts from deceased and living donors.

Mean age of transplant recipients in the included studies ranged from 30 to 68 years (median 44); the majority of patients were male (median 62%). We collected data on the proportion of patients in each group who had diabetes, coronary artery disease, hypertension, heart failure, stroke, lung disease, peripheral vascular disease, malignancy, infectious disease and smoking status. Unfortunately, these data were reported very infrequently and so are not reported here. Characteristics that were explored by the included studies as potential determinants of the benefit of transplantation were hepatitis B and/or hepatitis C virus serostatus of the recipient (13,14) and donor (15), extended-criteria donor (16,17), primary cause of ESRD (18–23), findings of coronary angiography (24,25), coronary artery bypass surgery (26), a low-protein diet (27), cancer (28), diabetes (22,29–34), obesity (35), employment (36), race (37–42) and age (7,43–47).

Risk of bias assessment

All eligible studies used a cohort design: 26% were prospective, 36% were based on registries with prospectively collected data, 2% were ambispective (both prospective and retrospective data collection), 18% were retrospective and 13% did not specify the relative timing of hypothesis generation and data collection. The risk of bias of included studies is reported in Table S2 and summarized in Figure 2.

Mortality

In all, 163 cohorts (77 studies; 1 800 119 participants) reported unadjusted comparisons of mortality associated with transplantation as compared with dialysis. Of these, 76% found a significantly lower risk of death associated with transplantation and 7% found a significantly lower risk of death associated with dialysis (Figure S1).

Six studies (7,38,46,48–50; 19 945 participants) reported adjusted relative hazards for all-cause mortality in discrete time periods (Figure 3). During the period immediately after transplantation (five studies reported a time period of <30 days and one <3 months [48]), mortality tended to be significantly greater in transplant recipients (HR range 0.9–5.03). These studies also reported the relative hazard of mortality at 1 year after transplantation, which in all cases, was significantly lower among transplant recipients (HR range 0.19–0.49).

Thirty-eight cohorts (8,15,17,19,21,30,31,35,37,42–44,51–61; 23 studies; 904 610 participants) reported adjusted relative hazards, rates or odds for mortality during total follow-up after transplantation (maximum follow up ranged 6–19 years; Figure 3). Seventy-nine percent of these results significantly favored lower mortality in the transplantation groups (HR range 0.16–0.76) and 21% were nonsignificant (HR range 0.33–1.12). These studies also included perioperative deaths, and thus, demonstrate that the higher short-term risk of death associated with kidney transplantation is more than offset by the lower risk of mortality during subsequent follow up. In the subset of studies including only waitlisted participants (10 studies; 474 522 participants), 94% of comparisons significantly favored lower mortality for transplant recipients (15 of 16 comparisons; HR range 0.16–0.73).

Three studies (35,58,60) reported relative hazards separately for living donor transplantation and for deceased donor transplantation, and found that the relative hazards of transplantation, compared to dialysis, tended to be lower for analyses of living donors (HR 0.23, 0.33 and 0.55) than for analyses of deceased donors (0.39, 1.12 and 1.01, respectively). However, given the small number of studies, no firm conclusions can be drawn from these results.

Evidence of effect modification for mortality

In multivariable meta-regression of 20 studies (13,27,51–55,63–74; 865 208 participants), we found that the unadjusted relative risk of mortality associated with transplantation (compared with dialysis) was lower in more recently performed studies (p < 0.001; Figure 4, panel A). Results were similar when a subset of 10 studies (7,19,46,56,76–79), including only 97 873 dialysis patients who had been placed on the transplant waiting list, were considered (p = 0.12; Figure 4, panel B). Variables assessing risk of bias (i.e. study design [prospective, registry, etc.], adequate description of population, prevalent vs. incident patients, censoring at modality switch and funding) were not significantly associated with the benefit of transplantation in meta-regression. Other variables were not tested as they were not relevant to the unadjusted mortality results (e.g. outcome definitions, adjusted model) or they did not sufficiently differ in value (e.g. contemporaneous groups).

Limited information was available on characteristics modifying the association between transplantation and mortality. One study (60) tested whether age, the number of associated diseases and dialysis vintage affected the association between transplantation and mortality, but found no significant evidence of effect modification. Another study (61) also tested the association between age and the mortality benefit of transplantation, but found no significant effect modification. A third study (31) found that the reduction in mortality associated with transplantation was greater among patients with peripheral arterial disease than in those without. We found no evidence that the association between transplantation and mortality was modified by dialytic modality.

Overall, there was no consistent association between markers of study risk of bias and the magnitude of the mortality reduction associated with transplantation. However, the benefits of transplantation seemed less pronounced in the subset of studies that were restricted to patients who were waitlisted for transplantation.

Meta-regression did not identify factors that significantly modified the association between transplantation and clinical outcomes other than mortality.

Cardiovascular events and hospitalization

In unadjusted analyses, four of six cohorts (19,20,25,33; four studies; 189 769 participants) found that transplantation significantly reduced the risk of myocardial infarction; two of five cohorts (19,20,56; three studies; 190 109 participants) found that transplantation significantly reduced the risk of stroke and two further studies found that transplantation significantly reduced the risk of heart failure (11 369 participants [18]) and the incidence of ischemic heart disease (552 participants [56]). Only two studies reported adjusted analyses for cardiac events. One (19; 92 participants) found that transplantation from a deceased donor significantly reduced the rate of cardiac events by 76% (relative rate 0.24, 95% CI: 0.07–0.81) and the other (18; 11 369 participants) found no association between transplantation and heart failure. The risk of infection-related hospitalization seemed to be significantly decreased among transplant recipients, with both cohorts (one study; 336 986 participants) favoring transplantation. Results for all-cause hospitalization were more equivocal, with only 5 of 10 cohorts (six studies; 354 256 participants) significantly favoring transplantation. Results of these analyses are summarized in Figure 5.

Quality of life

In unadjusted analyses comparing QoL using the SF-36 between transplant recipients and dialysis patients, 47–100% of cohorts (55,80–87; depending on the domain considered), significantly favored the transplantation groups and none significantly favored the dialysis groups. Three cohorts (80,88; two studies; 497 participants) reported the adjusted association between transplantation and SF-36 scores as compared with dialysis. The vast majority of analyses significantly favored transplantation over hemodialysis. One small cohort (80; 64 participants) comparing transplantation to peritoneal dialysis was not significantly different for any of the domains reported. These findings are summarized in Figure 6. Results were broadly similar for unadjusted and adjusted analyses comparing QoL assessed using other instruments including EQ-5D, Karnofsky Performance Index, SIP, GHQ, WHO-QoL, 15D and TTO (data not shown).

Discussion

In this systematic review of 110 studies including a total of 1 961 904 participants with kidney failure, kidney transplantation was associated with reduced risk of mortality and cardiovascular events as well as better QoL than treatment with chronic dialysis. Results were consistent for different dialysis modalities, for transplantation from both deceased and living donors and across countries with differing health care systems. These results confirm that kidney transplantation is the preferred modality of treatment for chronic kidney failure, and justifies current attempts to increase the number of patients worldwide who benefit from kidney transplantation—by increasing rates of deceased and living kidney donation, expanding the pool of potential donors and recipients and reducing the likelihood that potentially viable organs are discarded.

As expected, mortality among transplant recipients increased sharply as compared with those remaining on dialysis during the perioperative period (62). Thereafter, mortality among transplant recipients significantly declined such that cumulative mortality associated with transplantation was significantly lower than among patients treated with dialysis (62,89). Contemporary dialysis patients have more comorbidity and must wait longer for transplantation than patients awaiting kidney transplantation in previous years (6). Despite this, our results suggest that the relative benefit of transplantation may have significantly increased over time, compared to remaining on dialysis. For example, the unadjusted relative risk of mortality associated with transplantation (compared with dialysis) decreased from 0.44 in 1985 to 0.17 in 2005. This finding may relate to use of more potent immunosuppression, better management of comorbid medical conditions, more careful selection of transplant recipients or perhaps, to highe mortality in more recent years among the comparator pool of patients remaining on dialysis (89–91). However, because our study did not identify the explanation for this finding, these suggestions are speculative. Alternatively, because the apparently greater benefit of transplantation in more recent years was based on unadjusted analyses, it is possible that confounding by comorbidity or other characteristics wholly or partially explains this finding. Finally, we used the median year of each study's accrual period as a proxy for era of transplantation—which may have led to the ecological fallacy. Therefore, although appealing, our conclusion that the relative benefit of transplantation has increased over time should be viewed with caution.

Immunosuppressive medications used in transplant recipients may cause anemia, hypertension, glucose intolerance and dyslipidemia (91). Despite this, in analyses based on a total of 10 studies (333 881 patients), we found that transplantation was associated with significantly lower risk of cardiovascular events compared to treatment with dialysis (18–20,25,33,56). Although this finding might be partially because of selection of healthier patients for transplantation, results were similar in analyses restricted to dialysis patients who were active on the transplant waiting list—which should minimize the effect of such bias. Although immunosuppressive medications can predispose to infection, our results suggest that transplantation is associated with reduced risk of hospitalization for infection—emphasizing the high risk of sepsis associated with vascular and peritoneal access required to perform dialysis. We did not find clear evidence that transplant recipients were at lower risk of all-cause hospitalization than dialysis patients, perhaps because allograft recipients require hospitalization for transplantation itself as well as any surgical complications.

We found consistent and clinically relevant improvements in QoL associated with kidney transplantation (78,86,92). These results were consistent across a variety of settings, were preserved in adjusted analyses, and were observed for a broad range of QoL instruments (78,86,92,93). Because markedly reduced QoL is a hallmark of kidney failure, these improvements may be the most important benefit of kidney transplantation, compared with remaining on dialysis.

Although one of the major objectives of our study was to examine factors that modified the clinical benefits of transplantation (as compared to dialysis), we identified few data addressing this objective. However, findings from a single study (with 96 736 participants) suggested that the mortality reduction associated with transplantation was more pronounced in patients with peripheral arterial disease. Meta-regression was unhelpful for identifying factors that modified the association between transplantation and outcomes other than mortality.

To our knowledge, this is the most comprehensive and up-to-date summary of the potential benefits of kidney transplantation, as compared with dialysis. We used a carefully designed literature search and rigorous methods to capture and synthesize the results of 110 studies, published over a period of more than four decades. Our results clearly illustrate the clinical benefits of kidney transplantation. Together with the dismal outcomes associated with dialysis and the dramatic worldwide increases in projected waiting times for kidney transplantation among patients with kidney failure, these findings emphasize the urgent need to increase rates of deceased and living kidney donation (94).

As with all systematic reviews, the strength of our conclusions is dependent on the analysis of aggregate (study-level) data and the quality and availability of studies. In addition to assessing studies for bias using items from Downs and Black (11), we added specific items of bias pertinent to our question. Second, we found a significant increase in the benefit of kidney transplantation over time, perhaps because of improvements in the care of transplant recipients. Unfortunately, despite our best efforts, we were unable to identify patient-level or study-level factors that were associated with greater or lesser benefit from transplantation. Third, although we sought to determine a summary estimate of the benefit of kidney transplantation for clinically relevant outcomes, there was substantial heterogeneity in all pooled analyses (I²≥ 97%), making the validity of meta-analysis questionable. Despite use of meta-regression, we were unable to explain the source of this heterogeneity—which may be because of the wide range of renal replacement modalities we included, to the observational nature of the various studies, to the ecological fallacy (95) or to the fact that some (but not all) studies included dialysis patients who were not eligible for transplantation (selection bias). However, the magnitude and consistency of the benefit associated with transplantation across analyses leave little doubt that transplantation is beneficial as compared with dialysis, even if this benefit cannot be easily conveyed in a single summary measure. Finally, because multiple studies from certain countries were captured by our search, it is possible that a small minority of patients were included in more than one study. Because we did not statistically pool results across studies and because results were consistent for all analyses, this is unlikely to have affected our results.

Given the scarcity of renal allografts, future studies should explicitly seek to identify patient-level factors associated with the benefit of transplantation for outcomes other than mortality. For some outcomes (such as cardiovascular events or all-cause hospitalization), this could be achieved by patient-level meta-analysis (perhaps of registry data from different countries), which would increase statistical power and also reduce the risk of the ecological fallacy. Other outcomes (such as QoL) will require detailed prospective study, perhaps in conjunction with data collected to determine candidacy for transplantation. Because statistical adjustment for potential confounders will be critical for the success of such initiatives, consensus on the best way to measure and adjust for comorbidity, accruing after wait-listing for transplantation, would be an important next step.

In summary, we found that (as compared with dialysis), kidney transplantation is associated with substantial reductions in the risk of mortality and cardiovascular events, as well as clinically relevant improvements in QoL. Despite increases in the age and comorbidity of contemporary transplant recipients, the relative benefits of transplantation (as compared to remaining on dialysis) seem to be increasing over time. Given the current organ shortage, these findings validate current attempts to increase the number of people worldwide that benefit from kidney transplantation.

Acknowledgments

The authors sincerely thank Ellen Crumley for librarian support, Ghenette Houston for administrative support, Mohammad Karkhaneh, Natasha Krahn and Sophanny Tiv for additional reviewer support.

Funding source: This study was funded by the Canadian Institutes of Health Research. Drs. Tonelli and Klarenbach were supported by salary awards from the Alberta Heritage Foundation for Medical Research. Dr. Tonelli was also supported by a Government of Canada Research Chair in the optimal care of people with chronic kidney disease. Drs. Tonelli and Klarenbach were supported by a joint initiative between Alberta Health and Wellness and the Universities of Alberta and Calgary. Dr. Gill was supported by a salary award from the Michael Smith Foundation. Dr. Knoll is supported by a University of Ottawa Chair in Clinical Transplantation Research.

Authors’ contributions

M.T., G.K., S.K., J.G. and Ms. N.W. contributed to the design of the study. N.W. performed the statistical analyses and managed the project. M.T. wrote the first draft of the manuscript. All authors contributed to data acquisition, the interpretation of results and critical revision of the article for intellectually important content.

Disclosure

The authors of this manuscript have no conflicts of interest to disclose as described by the American Journal of Transplantation.

Supporting Information

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Volume11, Issue10

October 2011

Pages 2093-2109

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Systematic Review: Kidney Transplantation Compared With Dialysis in Clinically Relevant Outcomes