Polyclonal and monoclonal antibodies for treating acute rejection episodes in kidney transplant recipients

Angela C Webster; Sunny Wu; Krishna Tallapragada; Min Young Park; Jeremy R Chapman; Sue J Carr

doi:10.1002/14651858.CD004756.pub4

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Figure 1

Study flow diagram.

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Analysis 1.1

Comparison 1 Treatment of first rejection (T cell): antibody versus steroids (stratified by antibody type), Outcome 1 Failure of reversal of acute rejection.

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Analysis 1.2

Comparison 1 Treatment of first rejection (T cell): antibody versus steroids (stratified by antibody type), Outcome 2 Additional treatment needed.

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Analysis 1.3

Comparison 1 Treatment of first rejection (T cell): antibody versus steroids (stratified by antibody type), Outcome 3 Recurrent rejection up to 12 months post‐therapy.

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Analysis 1.4

Comparison 1 Treatment of first rejection (T cell): antibody versus steroids (stratified by antibody type), Outcome 4 Graft loss or death with a functioning graft within 12 months.

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Analysis 1.5

Comparison 1 Treatment of first rejection (T cell): antibody versus steroids (stratified by antibody type), Outcome 5 Graft loss censored for death within 18 months.

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Analysis 1.6

Comparison 1 Treatment of first rejection (T cell): antibody versus steroids (stratified by antibody type), Outcome 6 Death within 12 months.

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Analysis 1.7

Comparison 1 Treatment of first rejection (T cell): antibody versus steroids (stratified by antibody type), Outcome 7 Treatment adverse events.

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Analysis 1.8

Comparison 1 Treatment of first rejection (T cell): antibody versus steroids (stratified by antibody type), Outcome 8 Serum creatinine post treatment (3 months).

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Analysis 2.1

Comparison 2 Treatment of first rejection (T cell): antibody + steroids versus steroids alone, Outcome 1 Failure of reversal of acute rejection (AR) episode.

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Analysis 2.2

Comparison 2 Treatment of first rejection (T cell): antibody + steroids versus steroids alone, Outcome 2 Recurrent rejection within 3 months post‐therapy.

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Analysis 2.3

Comparison 2 Treatment of first rejection (T cell): antibody + steroids versus steroids alone, Outcome 3 Graft loss or death with a functioning graft within 12 months.

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Analysis 2.4

Comparison 2 Treatment of first rejection (T cell): antibody + steroids versus steroids alone, Outcome 4 Graft loss censored for death within 12 months.

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Analysis 2.5

Comparison 2 Treatment of first rejection (T cell): antibody + steroids versus steroids alone, Outcome 5 Death within 12 months.

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Analysis 3.1

Comparison 3 Treatment of first rejection (T cell): muromonab‐CD3 versus other antibody (stratified by comparator), Outcome 1 Failure of acute rejection reversal.

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Analysis 3.2

Comparison 3 Treatment of first rejection (T cell): muromonab‐CD3 versus other antibody (stratified by comparator), Outcome 2 Additional treatment needed.

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Analysis 3.3

Comparison 3 Treatment of first rejection (T cell): muromonab‐CD3 versus other antibody (stratified by comparator), Outcome 3 Recurrent rejection up to 12 months post‐therapy.

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Analysis 3.4

Comparison 3 Treatment of first rejection (T cell): muromonab‐CD3 versus other antibody (stratified by comparator), Outcome 4 Treatment adverse events.

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Analysis 4.1

Comparison 4 Treatment of first rejection (B cell): rituximab + steroids versus steroids alone, Outcome 1 Failure of reversal of acute rejection.

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Analysis 4.2

Comparison 4 Treatment of first rejection (B cell): rituximab + steroids versus steroids alone, Outcome 2 Additional treatment required.

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Analysis 4.3

Comparison 4 Treatment of first rejection (B cell): rituximab + steroids versus steroids alone, Outcome 3 Graft loss or death with a functioning graft within 12 months.

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Analysis 4.4

Comparison 4 Treatment of first rejection (B cell): rituximab + steroids versus steroids alone, Outcome 4 Death within 12 months.

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Analysis 4.5

Comparison 4 Treatment of first rejection (B cell): rituximab + steroids versus steroids alone, Outcome 5 Treatment adverse events.

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Analysis 5.1

Comparison 5 Treatment of steroid‐resistant rejection: antibody versus other antibody (stratified by antibody type), Outcome 1 Failure of acute rejection reversal.

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Analysis 5.2

Comparison 5 Treatment of steroid‐resistant rejection: antibody versus other antibody (stratified by antibody type), Outcome 2 Additional treatment required.

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Analysis 5.3

Comparison 5 Treatment of steroid‐resistant rejection: antibody versus other antibody (stratified by antibody type), Outcome 3 Recurrent rejection.

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Analysis 5.4

Comparison 5 Treatment of steroid‐resistant rejection: antibody versus other antibody (stratified by antibody type), Outcome 4 Graft loss censored for death (< 1 year).

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Analysis 5.5

Comparison 5 Treatment of steroid‐resistant rejection: antibody versus other antibody (stratified by antibody type), Outcome 5 Graft loss or death with a functioning graft (< 1 year).

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Analysis 5.6

Comparison 5 Treatment of steroid‐resistant rejection: antibody versus other antibody (stratified by antibody type), Outcome 6 Death within 12 months.

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Analysis 5.7

Comparison 5 Treatment of steroid‐resistant rejection: antibody versus other antibody (stratified by antibody type), Outcome 7 Treatment adverse events.

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Analysis 5.8

Comparison 5 Treatment of steroid‐resistant rejection: antibody versus other antibody (stratified by antibody type), Outcome 8 Serum creatinine post treatment (3 days).

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Analysis 5.9

Comparison 5 Treatment of steroid‐resistant rejection: antibody versus other antibody (stratified by antibody type), Outcome 9 Serum creatinine at 12 months.

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Summary of findings for the main comparison. Antibody (T cell) versus steroid (stratified by antibody type) for the treatment of first rejection episodes in kidney transplant recipients

Antibody (T cell) versus steroid (stratified by antibody type) for the treatment of first rejection episodes in kidney transplant recipients
Patient or population: kidney transplant recipients: first rejection episode Setting: single and multicentre Intervention: antibody (T cell) Comparison: steroid (stratified by antibody type)
Outcomes	*Anticipated absolute effects^ (95% CI)**		Relative effect (95% CI)	No. of participants (studies)	Quality of the evidence (GRADE)
	Risk with steroid (stratified by antibody type)	Risk with antibody (T cell)
Failure of reversal of acute rejection	Study population		RR 0.50 (0.30 to 0.82)	405 (6)	⊕⊕⊕⊝ MODERATE ¹
	342 per 1,000	171 per 1,000 (102 to 280)
Recurrent rejection Follow up: 12 months	Study population		RR 0.75 (0.56 to 1.00)	508 (9)	⊕⊕⊕⊝ MODERATE ¹
	566 per 1,000	425 per 1,000 (317 to 566)
Graft loss or death with a functioning graft Follow up: 12 months	Study population		RR 0.84 (0.58 to 1.22)	490 (8)	⊕⊕⊝⊝ LOW ^{1 2}
	459 per 1,000	385 per 1,000 (266 to 560)
Graft loss censored for death Follow up: 18 months	Study population		RR 0.80 (0.57 to 1.12)	475 (8)	⊕⊕⊝⊝ LOW ^{1 2}
	409 per 1,000	327 per 1,000 (233 to 458)
Death Follow up: 12 months	Study population		RR 0.98 (0.51 to 1.88)	413 (7)	⊕⊝⊝⊝ VERY LOW ^{1 3}
	83 per 1,000	81 per 1,000 (42 to 155)
Treatment adverse events: fever, chill, or malaise after drug administration	Study population		RR 23.88 (5.10 to 111.86)	280 (4)	⊕⊝⊝⊝ VERY LOW ^{1 3 4}
	0 per 1,000	0 per 1,000 (0 to 0)
*The risk in the intervention group (and its 95% CI) is based on the assumed risk in the comparison group and the relative effect of the intervention (and its 95% CI). CI: Confidence interval; RR: Risk ratio
GRADE Working Group grades of evidence High quality: We are very confident that the true effect lies close to that of the estimate of the effect Moderate quality: We are moderately confident in the effect estimate: The true effect is likely to be close to the estimate of the effect, but there is a possibility that it is substantially different Low quality: Our confidence in the effect estimate is limited: The true effect may be substantially different from the estimate of the effect Very low quality: We have very little confidence in the effect estimate: The true effect is likely to be substantially different from the estimate of effect
¹ Unclear/high risk in multiple studies for allocation concealment and selective reporting ² CI includes null effect and potential for some harm and benefit ³ CI includes null effect and appreciable harm and benefit ⁴ High I² (81%) and great variation in size of effect across all different treatment adverse effects

Summary of findings for the main comparison. Antibody (T cell) versus steroid (stratified by antibody type) for the treatment of first rejection episodes in kidney transplant recipients

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Summary of findings 2. Antibody (T cell) + steroid versus steroid alone for the treatment of first rejection episodes in kidney transplant recipients

Antibody (T cell) + steroid versus steroid alone for the treatment of first rejection episodes in kidney transplant recipients
Patient or population: treatment of first rejection episodes in kidney transplant recipients: first rejection episode Setting: single centre Intervention: antibody (T cell) + steroid Comparison: steroid alone
Outcomes	*Anticipated absolute effects^ (95% CI)**		Relative effect (95% CI)	No. of participants (studies)	Quality of the evidence (GRADE)
	Risk with steroid alone	Risk with antibody (T cell) + steroid
Failure of reversal of acute rejection episode	Study population		RR 0.42 (0.17 to 1.01)	30 (1)	⊕⊕⊝⊝ LOW ^{1 2 3}
	688 per 1,000	289 per 1,000 (117 to 694)
Recurrent rejection Follow up: 3 months	Study population		RR 0.07 (0.00 to 1.06)	30 (1)	⊕⊕⊝⊝ LOW ^{1 2 3}
	500 per 1,000	35 per 1,000 (0 to 530)
Graft loss or death with a functioning graft Follow up: 12 months	Study population		RR 0.35 (0.02 to 5.14)	52 (2)	⊕⊝⊝⊝ VERY LOW ^{1 3 4 5}
	346 per 1,000	121 per 1,000 (7 to 1,000)
Graft loss censored for death Follow up: 12 months	Study population		RR 0.33 (0.03 to 4.16)	50 (2)	⊕⊝⊝⊝ VERY LOW ^{1 3 4 5}
	385 per 1,000	127 per 1,000 (12 to 1,000)
Death Follow up: 12 months	Study population		RR 0.86 (0.53 to 1.39)	50 (2)	⊕⊕⊝⊝ LOW ^{1 3 6}
	462 per 1,000	397 per 1,000 (245 to 642)
*The risk in the intervention group (and its 95% CI) is based on the assumed risk in the comparison group and the relative effect of the intervention (and its 95% CI). CI: Confidence interval; RR: Risk ratio
GRADE Working Group grades of evidence High quality: We are very confident that the true effect lies close to that of the estimate of the effect Moderate quality: We are moderately confident in the effect estimate: The true effect is likely to be close to the estimate of the effect, but there is a possibility that it is substantially different Low quality: Our confidence in the effect estimate is limited: The true effect may be substantially different from the estimate of the effect Very low quality: We have very little confidence in the effect estimate: The true effect is likely to be substantially different from the estimate of effect
¹ Small sample size and few number of events ² Width of CI is very wide. CI includes null effect and is strongly one‐sided. ³ Unclear risk for random sequence generation and allocation concealment, and high risk for selective reporting ⁴ Big variation in size of effect with small overlap of CI and high I² value ⁵ Width of CI is very wide. CI includes both null effect and appreciable benefit and harm ⁶ CI includes both null effect and appreciable benefit and harm

Summary of findings 2. Antibody (T cell) + steroid versus steroid alone for the treatment of first rejection episodes in kidney transplant recipients

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Summary of findings 3. Muromonab‐CD3 (T cell) versus other antibody (stratified by comparator) for the treatment of first rejection episodes in kidney transplant recipients

Muromonab‐CD3 (T cell) versus other antibody (stratified by comparator) for the treatment of first rejection episodes in kidney transplant recipients
Patient or population: kidney transplant recipients: first rejection episode Setting: single centre Intervention: muromonab‐CD3 (T cell) Comparison: other antibody (stratified by comparator)
Outcomes	*Anticipated absolute effects^ (95% CI)**		Relative effect (95% CI)	No. of participants (studies)	Quality of the evidence (GRADE)
	Risk with other antibody (stratified by comparator)	Risk with muromonab‐CD3 (T cell)
Failure of acute rejection reversal	Study population		RR 1.84 (0.92 to 3.67)	132 (2)	⊕⊕⊕⊝ MODERATE ^{1 2}
	134 per 1,000	247 per 1,000 (124 to 493)
Recurrent rejection Follow up: 12 months	Study population		RR 1.06 (0.59 to 1.88)	129 (2)	⊕⊕⊕⊝ MODERATE ^{1 2}
	254 per 1,000	269 per 1,000 (150 to 477)
Treatment adverse events: fever, chills, malaise after drug administration	Study population		RR 3.12 (1.87 to 5.21)	132 (2)	⊕⊕⊝⊝ LOW ^{1 3}
	269 per 1,000	838 per 1,000 (502 to 1,000)
Treatment adverse events: neurological side effects	Study population		RR 13.10 (1.43 to 120.05)	132 (2)	⊕⊕⊝⊝ LOW ^{1 3}
	15 per 1,000	196 per 1,000 (21 to 1,000)
*The risk in the intervention group (and its 95% CI) is based on the assumed risk in the comparison group and the relative effect of the intervention (and its 95% CI). CI: Confidence interval; RR: Risk ratio
GRADE Working Group grades of evidence High quality: We are very confident that the true effect lies close to that of the estimate of the effect Moderate quality: We are moderately confident in the effect estimate: The true effect is likely to be close to the estimate of the effect, but there is a possibility that it is substantially different Low quality: Our confidence in the effect estimate is limited: The true effect may be substantially different from the estimate of the effect Very low quality: We have very little confidence in the effect estimate: The true effect is likely to be substantially different from the estimate of effect
¹ Small sample size and few number of events ² CI includes null effect and potential for some harm and benefit ³ High I² value and wide variation in size of effect

Summary of findings 3. Muromonab‐CD3 (T cell) versus other antibody (stratified by comparator) for the treatment of first rejection episodes in kidney transplant recipients

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Summary of findings 4. Rituximab (B cell) + steroid versus steroid alone for the treatment of first rejection episodes in kidney transplant recipients

Rituximab (B cell) + steroid versus steroid alone for the treatment of first rejection episodes in kidney transplant recipients
Patient or population: kidney transplant recipients: first rejection episode Setting: single and multicentre Intervention: rituximab (B cell) + steroid Comparison: steroid alone
Outcomes	*Anticipated absolute effects^ (95% CI)**		Relative effect (95% CI)	No. of participants (studies)	Quality of the evidence (GRADE)
	Risk with steroid alone	Risk with rituximab (B cell) + steroid
Failure of reversal of acute rejection	Study population		RR 0.94 (0.54 to 1.64)	53 (2)	⊕⊕⊕⊝ MODERATE ^{1 2}
	500 per 1,000	470 per 1,000 (270 to 820)
Graft loss or death with a functioning graft Follow up: 12 months	Study population		RR 1.00 (0.23 to 4.35)	58 (2)	⊕⊕⊕⊝ MODERATE ^{1 2}
	103 per 1,000	103 per 1,000 (24 to 450)
Death Follow up: 12 months	Study population		not estimable	58 (2)	⊕⊕⊕⊕ HIGH
	0 per 1,000	0 per 1,000 (0 to 0)
Treatment adverse events: UTI/pyelonephritis	Study population		RR 5.73 (1.80 to 18.21)	38 (1)	⊕⊕⊕⊝ MODERATE ¹
	111 per 1,000	637 per 1,000 (200 to 1,000)
*The risk in the intervention group (and its 95% CI) is based on the assumed risk in the comparison group and the relative effect of the intervention (and its 95% CI). CI: Confidence interval; RR: Risk ratio
GRADE Working Group grades of evidence High quality: We are very confident that the true effect lies close to that of the estimate of the effect Moderate quality: We are moderately confident in the effect estimate: The true effect is likely to be close to the estimate of the effect, but there is a possibility that it is substantially different Low quality: Our confidence in the effect estimate is limited: The true effect may be substantially different from the estimate of the effect Very low quality: We have very little confidence in the effect estimate: The true effect is likely to be substantially different from the estimate of effect
¹ Small sample size and few number of events ² CI includes both null effect and appreciable benefit and harm

Summary of findings 4. Rituximab (B cell) + steroid versus steroid alone for the treatment of first rejection episodes in kidney transplant recipients

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Summary of findings 5. Antibody versus other antibody (stratified by antibody type) for the treatment of steroid‐resistant rejection episodes in kidney transplant recipients

Antibody versus other antibody (stratified by antibody type) for the treatment of steroid‐resistant rejection episodes in kidney transplant recipients
Patient or population: kidney transplant recipients: steroid‐resistant rejection episodes Setting: single centre Intervention: antibody Comparison: other antibody (stratified by antibody type)
Outcomes	*Anticipated absolute effects^ (95% CI)**		Relative effect (95% CI)	No. of participants (studies)	Quality of the evidence (GRADE)
	Risk with other antibody (stratified by antibody type)	Risk with antibody
Failure of acute rejection reversal	Study population		RR 1.07 (0.63 to 1.81)	244 (5)	⊕⊕⊝⊝ LOW ^{1 2}
	206 per 1,000	221 per 1,000 (130 to 373)
Recurrent rejection	Study population		RR 0.78 (0.47 to 1.28)	284 (5)	⊕⊕⊝⊝ LOW ^{1 2}
	356 per 1,000	278 per 1,000 (167 to 456)
Graft loss censored for death Follow up: 12 months	Study population		RR 0.86 (0.34 to 2.17)	244 (5)	⊕⊕⊝⊝ LOW ^{1 2}
	183 per 1,000	157 per 1,000 (62 to 396)
Graft loss or death with a functioning graft Follow up: 12 months	Study population		RR 0.81 (0.43 to 1.51)	211 (5)	⊕⊕⊝⊝ LOW ^{1 2}
	229 per 1,000	186 per 1,000 (99 to 346)
Death Follow up: 12 months	Study population		RR 0.39 (0.09 to 1.65)	175 (3)	⊕⊕⊝⊝ LOW ^{1 2 3}
	68 per 1,000	27 per 1,000 (6 to 112)
Treatment adverse events: fever, chills, malaise after drug administration	Study population				⊕⊕⊝⊝ LOW ^{1 4}
	342 per 1,000	870 per 1,000 (62 to 1,000)	RR 2.54 (0.18 to 34.92)	140 (3)
Treatment adverse events: bacterial infection	Study population		RR 8.64 (1.64 to 45.56)	109 (2)	⊕⊝⊝⊝ VERY LOW ^{2 3}
	17 per 1,000	149 per 1,000 (28 to 786)
*The risk in the intervention group (and its 95% CI) is based on the assumed risk in the comparison group and the relative effect of the intervention (and its 95% CI). CI: Confidence interval; RR: Risk ratio
GRADE Working Group grades of evidence High quality: We are very confident that the true effect lies close to that of the estimate of the effect Moderate quality: We are moderately confident in the effect estimate: The true effect is likely to be close to the estimate of the effect, but there is a possibility that it is substantially different Low quality: Our confidence in the effect estimate is limited: The true effect may be substantially different from the estimate of the effect Very low quality: We have very little confidence in the effect estimate: The true effect is likely to be substantially different from the estimate of effect
¹ CI includes both null effect and appreciable benefit and harm ² Unclear risk for random sequence generation and allocation across all studies ³ Small sample size and few number of events ⁴ High I² value and wide variation in size of effect

Summary of findings 5. Antibody versus other antibody (stratified by antibody type) for the treatment of steroid‐resistant rejection episodes in kidney transplant recipients

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Table 1. Inclusion criteria and outcome definitions used in studies of antibody for the treatment of first rejection episodes (cellular response)

Study ID	Days since transplant	Timing of randomisation	Criteria for rejection*	Criteria for rejection reversal*
Antibody versus steroid
Shield 1979	< 35	Rejection	Scoring algorithm of biochemical, and physical signs, with confirmatory “biopsy where possible”	Day 2 of “persistent creatinine fall”
Filo 1980	< 90	Rejection	“Clinical signs, imaging and renal function tests”	Increase in creatinine within 24 to 48 hours of bolus MP
Hoitsma 1982	< 90	Rejection	Increased creatinine, oliguria, sodium retention, weight gain, proteinuria, graft tenderness	Day 2 of 3 consecutive days of creatinine falling
Glass 1983	ns	Transplantation	Clinical criteria including creatinine rise for 3 sequential days	Improvement in creatinine and clinical signs at 7th day of treatment
Streem 1983	ns	Transplantation	Rise in creatinine and diminished function on I‐131 scan, with “supportive clinical findings” with confirmatory “biopsy where possible”	Day 2 of “persistent creatinine fall”
Goldstein 1985	6‐90	Rejection	Scoring algorithm of biochemical, and physical signs, with confirmatory “biopsy where possible”	3 day progressive fall in creatinine, or investigator judged clinical reversal.
Broyer 1987a	> 8	Rejection	“Rise in plasma creatinine” and “changes in kidney echogenicity” on ultrasound. If unsure, “rejection was confirmed by kidney biopsy”	ns
Hilbrands 1996	< 90	Rejection	ns	ns
Theodorakis 1998	ns	Rejection	Clinical ± biopsy confirmation	Not assessed. Severity of rejection episode judged by AUC of serial 10 day creatinine measurements.
Antibody and steroid versus steroid alone
Birkeland 1975	ns	Rejection	“Common clinical criteria”, with biopsy where possible	Day 2 of progressive rise in creatinine clearance
Simonian 1983	ns	Rejection	ns	ns
Antibody versus other antibody
Toledo‐Pereyra 1985	ns	Transplantation	Primarily by laboratory signs of increase in SCr ≥ 0.3 mg/dL on any given day, or “clinical signs associated with rejection” and “an increase in kidney size on ultrasound”	ns
Waid 1991	ns	Rejection	4 of 7 clinical and biochemical signs, subsequently confirmed by biopsy	Absence of cross‐over, re‐treatment or graft loss
Baldi 2000	ns	Rejection	20% increase in creatinine with clinical suggestive signs, and biopsy if > 10 days from transplantation	ns
Formulation comparisons
Johnson 1989	ns	Rejection	Standard clinical indicators with supplementary “biopsy where possible”	1st of 3 consecutive days of creatinine falling
Antibody versus other treatment
Howard 1977	ns	Rejection	Rise in creatinine of 0.3 mg/dL and deterioration of renogram, “mostly confirmed by biopsy”	ns
Hourmant 1985	> 90	90 days post‐transplant	ns	ns
* direct quotation from the text of study reports appears in quotation marks AUC ‐ area under the curve; ns ‐ not stated and could not be clarified or deduced; MP ‐ methylprednisolone; SCr ‐ serum creatinine

Table 1. Inclusion criteria and outcome definitions used in studies of antibody for the treatment of first rejection episodes (cellular response)

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Table 2. Inclusion criteria and outcome definitions used in studies of antibody for the treatment of first rejection episodes (humoral response)

Study ID	Days since transplant*	Timing of randomisation*	Criteria for rejection*	Criteria for rejection reversal*
Antibody versus placebo
Zarkhin 2008	ns	Rejection	“Biopsy proven” and Banff graded	“Recovery of graft function to within 20% of the baseline pre‐rejection value 1, 3, 6, and 12 months after the episode”, and “Resolution of the Banff biopsy grade”
RITUX‐ERAH 2016	ns	Rejection	“Biopsy proven”	“Improvement of renal function at day 12”
* direct quotation from the text of study reports appears in quotation marks MP ‐ methylprednisolone; ns ‐ not stated and could not be clarified or deduced

Table 2. Inclusion criteria and outcome definitions used in studies of antibody for the treatment of first rejection episodes (humoral response)

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Table 3. Inclusion criteria and outcomes definitions used in studies of antibody for the treatment of resistant rejection episodes

Study ID	Days since transplant*	Timing of randomisation*	Criteria for rejection*	Initial treatment of rejection*	Criteria for resistant rejection*
Antibody versus other antibody
Blumke 1989	ns	“Steroid resistant rejection crisis”	ns	3 bolus injections of cortisone	“Not sufficiently treated” with steroids
Campistol 1990	ns	ns	Confirmed by renal biopsy	MP 1g for 3 days	ns
Hesse 1990	< 42	ns	Rise in creatinine of > 0.3 mg/dL and biopsy	MP 500 mg for 2 days	“Non response”
Spieker 1992	“early”	ns	“Typical clinical symptoms”, renogram, and biopsy	MP 500‐1000 mg for 3 days	Lack of improvement in clinical and sonographic appearances
Alamartine 1994	ns	At biopsy	Biopsy with “histological diagnosis”	MP 15 mg/kg, 2 bolus doses	“Absence of a clear response to the steroids”
Mariat 1998	ns	At biopsy	Delayed graft function or rise in creatinine in presence of urine output < 1 L/d, low sodium excretion, weight gain > 1 kg/d or graft tenderness	MP 15 mg/kg, 2 doses alternate days	No decline in creatinine after 2 steroid boluses, followed by biopsy
Midtvedt 2003	ns	Day 5 of treatment	Rise in creatinine > 20% in the absence of obvious cause and biopsy (Banff criteria)	MP 500 mg then 250 mg for 3 days	No decline in creatinine
Different formulations of antibody
Gaber 1998	ns	At biopsy	Biopsy, Banff graded	MP 500 mg, for 3 days	Creatinine increase of 10% after 3 days of MP
Different doses of same antibody
Midtvedt 1996	< 90	Day 5 of treatment	Rise in creatinine > 20% in absence of obvious cause	MP boluses, cumulative dose 1‐1.5 g	No decline in creatinine after 5 days of treatment
Different duration of same antibody
Olausson 1995	ns	At biopsy	“Diagnosed clinically and verified with a core needle biopsy”	MP 250‐500 mg, for 4 days	Not responding with improved kidney function on 5th day of steroid treatment
Antibody versus other treatment
Okubo 1993	< 365	Day 4 of treatment	Accelerated rejection: “progressive rise in SCr level was observed within 7 days of transplant”. Acute rejection: “rise in SCr of 0.5 mg/dl or higher” was seen anytime during post‐transplant course. Acute on chronic rejection: “a similar rise in SCr occurred in a patient with sustained creatinine level of ≥2.5mg/dl due to a documented previous acute rejection episode”	MP 500‐1000 mg, for 3 days	“Serum creatinine did not revert to the basal level within a week from the onset”
Casadei 1998	ns	At biopsy	Clinical suspicion and biopsy	MP 500 mg for 3 days	“Failure to show improved renal function” within 7 days of starting MP
* direct quotation from the text of study reports appears in quotation marks MP ‐ methylprednisolone; ns ‐ not stated and could not be clarified or deduced

Table 3. Inclusion criteria and outcomes definitions used in studies of antibody for the treatment of resistant rejection episodes

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Table 4. Additional data and analysis (first rejection)

Outcomes	Comparisons Relative effect (95% CI)
Outcomes	rabbit‐ATG versus horse‐ATG (1 study, 159 participants)	ATG versus ALG (1 study, 50 participants)	ALG versus IVIg (1 study, 45 participants)
Failure of reversal of acute rejection	RR 0.88 (0.41 to 1.87)	RR 0.95 (0.28 to 3.27)	RR 2.40 (0.27 to 21.35)
Recurrent rejection post‐therapy	RR 1.24 (0.77 to 1.99)	RR: 0.95 (0.48 to 1.87)	RR 0.62 (0.28 to 1.38)
Graft loss or death with a functioning graft (≤ 12 months)	RR 0.73 (0.37 to 1.44)	RR 1.09 (0.60 to 1.99)	RR 1.00 (0.49 to 2.05)
Graft loss censored for death (≤ 12 months)	Not reported	RR 0.89 (0.41 to 1.93)	RR 0.93 (0.37 to 2.34)
Death (≤ 12 months)	Not reported	RR 2.00 (0.40 to 9.95)	RR 1.20 (0.22 to 6.50)
Malignancy (total)	Not reported	Not reported	RR 2.42 (0.10 to 56.46)
Treatment side effects: fevers, chills, malaise following administration	RR 0.38 (0.27 to 0.54)	RR 0.75 (0.19 to 3.01)	Not reported
Treatment side effects: thrombocytopenia	Not reported	RR 1.00 (0.07 to 15.12)	Not reported
ALG ‐ antilymphocyte globulin; ATG ‐ antithymocyte globulin; CI ‐ confidence interval; IVIg ‐ intravenous immunoglobulin; RR ‐ risk ratio

Table 4. Additional data and analysis (first rejection)

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Table 5. Additional data and analysis (steroid‐resistant rejection)

Outcome	Comparisons Relative effect (95% CI)
Outcome	rabbit‐ATG versus horse‐ATG (1 study, 163 participants)	ATG 3 days versus ALG 10 days (1 study, 30 participants)	Muromonab‐CD3half dose versus standard dose (1 study, 45 participants)	Muromonab‐CD3versus IVIg (1 study, 30 participants)	Muromonab‐CD3versus DSP (1 study, 25 participants)
Failure of reversal of acute rejection	RR 0.52 (0.26 to 1.05)	RR 0.88 (0.43 to 1.80)	RR 1.50 (0.29 to 7.73)	RR 0.50 (0.11 to 2.33)	RR 0.92 (0.35, 2.41)
Further treatment required	Not reported	RR 9.60 (0.56 to 163.58)	Not reported	Not reported	Not reported
Recurrent rejection post‐therapy	RR 0.32 (0.15 to 0.66)	Not reported	RR 0.50 (0.05 to 4.94)	RR 1.65 (0.80 to 3.41)	RR 1.48 (0.67 to 3.27)
Graft loss or death with a functioning graft (≤ 12 months)	RR 0.68 (0.37 to 1.26)	RR 0.86 (0.38 to 1.95)	RR 2.00 (0.43 to 9.32)	RR 1.00 (0.24 to 4.18)	Not reported
Graft loss censored for death (≤ 12 months)	RR 0.46 (0.21 to 1.00)	Not reported	RR 1.00 (0.16 to 6.20)	RR 2.00 (0.20 to 19.78)	Not reported
Death (≤ 12‐24 months)	RR 1.98 (0.51 to 7.63)	Not reported	RR 5.00 (0.26 to 96.13)	RR 0.50 (0.05 to 4.94)	Not reported
Treatment side effects: fevers, chills, malaise following administration	Not reported	Not reported	Not reported	RR 31.00 (2.02 to 475.12)	RR 5.54 (1.55 to 19.82)
Treatment side effects: leukopenia	RR 1.93 (1.32 to 2.84)	Not reported	Not reported	Not reported	RR 0.10 (0.02 to 0.69)
Treatment side effects: anorexia	Not reported	Not reported	Not reported	Not reported	RR 0.92 (0.15 to 5.56)
Treatment failure	RR 0.51 (0.25 to 1.04)	Not reported	Not reported	Not reported	Not reported
Infection (total)	RR 0.99 (0.73 to 1.34)	Not reported	Not reported	Not reported	Not reported
Infection (bacterial)	RR 0.79 (0.51 to 1.23)	Not reported	RR 3.00 (0.13 to 68.26)	Not reported	Not reported
Infection (viral)	RR 1.87 (0.88 to 3.94)	Not reported	Not reported	Not reported	Not reported
Infection (fungal)	RR 0.99 (0.36 to 2.69)	Not reported	Not reported	Not reported	Not reported
CMV infection (total)	RR 1.01 (0.86 to 1.18)	Not reported	RR 1.00 (0.51 to 1.95)	Not reported	Not reported
Malignancy (total)	RR 0.99 (0.21 to 4.75)	Not reported	Not reported	Not reported	Not reported
PTLD/Lymphoma	RR 1.48 (0.25 to 8.64)	Not reported	Not reported	Not reported	Not reported
SCr	Not reported	Not reported	MD ‐10.00 (‐60.15 to 40.15) (18 months after treatment)	MD 0.47 (‐0.07 to 1.01) (3 months after treatment)	MD 62.00 (‐107.08 to 231.08) (1 month after treatment)
ALG ‐ antilymphocyte globulin; ATG ‐ antithymocyte globulin; CI ‐ confidence interval; CMV ‐ cytomegalovirus; DSP ‐ 15‐deoxyspergualin; IVIg ‐ intravenous immunoglobulin; MD ‐ mean difference; PTLD ‐ post‐transplant lymphoproliferative disease; RR ‐ risk ratio; SCr ‐ serum creatinine

Table 5. Additional data and analysis (steroid‐resistant rejection)

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Comparison 1. Treatment of first rejection (T cell): antibody versus steroids (stratified by antibody type)

Outcome or subgroup title	No. of studies	No. of participants	Statistical method	Effect size
1 Failure of reversal of acute rejection Show forest plot	6	405	Risk Ratio (M‐H, Random, 95% CI)	0.50 [0.30, 0.82]

1.1 Muromonab‐CD3 versus steroid	1	122	Risk Ratio (M‐H, Random, 95% CI)	0.29 [0.14, 0.63]
1.2 ATG versus steroid	3	198	Risk Ratio (M‐H, Random, 95% CI)	0.40 [0.22, 0.74]
1.3 ALG versus steroid	2	85	Risk Ratio (M‐H, Random, 95% CI)	0.96 [0.52, 1.75]
2 Additional treatment needed Show forest plot	4	178	Risk Ratio (M‐H, Random, 95% CI)	0.74 [0.48, 1.15]

2.1 ATG versus steroid	2	120	Risk Ratio (M‐H, Random, 95% CI)	0.80 [0.49, 1.30]
2.2 ALG versus steroid	2	58	Risk Ratio (M‐H, Random, 95% CI)	0.50 [0.17, 1.49]
3 Recurrent rejection up to 12 months post‐therapy Show forest plot	9	508	Risk Ratio (M‐H, Random, 95% CI)	0.75 [0.56, 1.00]

3.1 Muromonab‐CD3 versus steroid	1	103	Risk Ratio (M‐H, Random, 95% CI)	0.89 [0.69, 1.15]
3.2 ATG versus steroid	5	285	Risk Ratio (M‐H, Random, 95% CI)	0.55 [0.29, 1.05]
3.3 ALG versus steroid	3	120	Risk Ratio (M‐H, Random, 95% CI)	0.87 [0.60, 1.28]
4 Graft loss or death with a functioning graft within 12 months Show forest plot	8	490	Risk Ratio (M‐H, Random, 95% CI)	0.84 [0.58, 1.22]

4.1 Muromonab‐CD3 versus steroid	1	120	Risk Ratio (M‐H, Random, 95% CI)	1.36 [1.02, 1.81]
4.2 ATG versus steroid	5	285	Risk Ratio (M‐H, Random, 95% CI)	0.65 [0.48, 0.89]
4.3 ALG versus steroid	2	85	Risk Ratio (M‐H, Random, 95% CI)	0.90 [0.53, 1.50]
5 Graft loss censored for death within 18 months Show forest plot	8	475	Risk Ratio (M‐H, Random, 95% CI)	0.80 [0.57, 1.12]

5.1 Muromonab‐CD3 versus steroid	1	120	Risk Ratio (M‐H, Random, 95% CI)	1.35 [0.94, 1.94]
5.2 ATG versus steroid	4	235	Risk Ratio (M‐H, Random, 95% CI)	0.63 [0.44, 0.89]
5.3 ALG versus steroid	3	120	Risk Ratio (M‐H, Random, 95% CI)	0.75 [0.42, 1.33]
6 Death within 12 months Show forest plot	7	413	Risk Ratio (M‐H, Random, 95% CI)	0.98 [0.51, 1.88]

6.1 Muromonab‐CD3 versus steroid	1	120	Risk Ratio (M‐H, Random, 95% CI)	1.40 [0.53, 3.70]
6.2 ATG versus steroid	3	173	Risk Ratio (M‐H, Random, 95% CI)	0.49 [0.14, 1.74]
6.3 ALG versus steroid	3	120	Risk Ratio (M‐H, Random, 95% CI)	1.05 [0.31, 3.60]
7 Treatment adverse events Show forest plot	5		Risk Ratio (M‐H, Random, 95% CI)	Subtotals only

7.1 Fever, chill, malaise after drug administration	4	280	Risk Ratio (M‐H, Random, 95% CI)	23.88 [5.10, 111.86]
7.2 Infection (total)	5	241	Risk Ratio (M‐H, Random, 95% CI)	0.83 [0.57, 1.20]
7.3 CMV infection	4	118	Risk Ratio (M‐H, Random, 95% CI)	0.92 [0.37, 2.26]
7.4 Avascular necrosis	3	143	Risk Ratio (M‐H, Random, 95% CI)	0.51 [0.11, 2.35]
8 Serum creatinine post treatment (3 months) Show forest plot	1	95	Mean Difference (IV, Random, 95% CI)	‐14.0 [‐37.53, 9.53]

Comparison 1. Treatment of first rejection (T cell): antibody versus steroids (stratified by antibody type)

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Comparison 2. Treatment of first rejection (T cell): antibody + steroids versus steroids alone

Outcome or subgroup title	No. of studies	No. of participants	Statistical method	Effect size
1 Failure of reversal of acute rejection (AR) episode Show forest plot	1		Risk Ratio (M‐H, Random, 95% CI)	Totals not selected

1.1 ALG + steroids versus steroids alone	1		Risk Ratio (M‐H, Random, 95% CI)	0.0 [0.0, 0.0]
2 Recurrent rejection within 3 months post‐therapy Show forest plot	1		Risk Ratio (M‐H, Random, 95% CI)	Totals not selected

2.1 ALG + steroids versus steroids alone	1		Risk Ratio (M‐H, Random, 95% CI)	0.0 [0.0, 0.0]
3 Graft loss or death with a functioning graft within 12 months Show forest plot	2	52	Risk Ratio (M‐H, Random, 95% CI)	0.35 [0.02, 5.14]

3.1 ALG + steroids versus steroids alone	1	32	Risk Ratio (M‐H, Random, 95% CI)	1.0 [0.24, 4.23]
3.2 ATG + steroids versus steroids alone	1	20	Risk Ratio (M‐H, Random, 95% CI)	0.08 [0.00, 1.21]
4 Graft loss censored for death within 12 months Show forest plot	2	50	Risk Ratio (M‐H, Random, 95% CI)	0.33 [0.03, 4.16]

4.1 ALG + steroids versus steroids alone	1	30	Risk Ratio (M‐H, Random, 95% CI)	0.86 [0.23, 3.19]
4.2 ATG + steroids versus steroids alone	1	20	Risk Ratio (M‐H, Random, 95% CI)	0.08 [0.00, 1.21]
5 Death within 12 months Show forest plot	2	50	Risk Ratio (M‐H, Random, 95% CI)	0.86 [0.53, 1.39]

5.1 ALG + steroids versus steroids alone	1	30	Risk Ratio (M‐H, Random, 95% CI)	0.86 [0.53, 1.39]
5.2 ATG + steroids versus steroids alone	1	20	Risk Ratio (M‐H, Random, 95% CI)	0.0 [0.0, 0.0]

Comparison 2. Treatment of first rejection (T cell): antibody + steroids versus steroids alone

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Comparison 3. Treatment of first rejection (T cell): muromonab‐CD3 versus other antibody (stratified by comparator)

Outcome or subgroup title	No. of studies	No. of participants	Statistical method	Effect size
1 Failure of acute rejection reversal Show forest plot	2	132	Risk Ratio (M‐H, Random, 95% CI)	1.84 [0.92, 3.67]

1.1 Muromonab‐CD3 versus ATG	1	56	Risk Ratio (M‐H, Random, 95% CI)	2.0 [0.95, 4.20]
1.2 Muromonab‐CD3 versus T10B9.1A‐31	1	76	Risk Ratio (M‐H, Random, 95% CI)	1.05 [0.16, 7.10]
2 Additional treatment needed Show forest plot	2	132	Risk Ratio (M‐H, Random, 95% CI)	1.67 [0.77, 3.63]

2.1 Muromonab‐CD3 versus ATG	1	56	Risk Ratio (M‐H, Random, 95% CI)	1.83 [0.79, 4.27]
2.2 Muromonab‐CD3 versus T10B9.1A‐31	1	76	Risk Ratio (M‐H, Random, 95% CI)	1.05 [0.16, 7.10]
3 Recurrent rejection up to 12 months post‐therapy Show forest plot	2	129	Risk Ratio (M‐H, Random, 95% CI)	1.06 [0.59, 1.88]

3.1 Muromonab‐CD3 versus ATG	1	53	Risk Ratio (M‐H, Random, 95% CI)	1.24 [0.61, 2.56]
3.2 Muromonab‐CD3 versus T10B9.1A‐31	1	76	Risk Ratio (M‐H, Random, 95% CI)	0.79 [0.30, 2.06]
4 Treatment adverse events Show forest plot	2		Risk Ratio (M‐H, Random, 95% CI)	Subtotals only

4.1 Fever, chills, malaise after drug administration	2	132	Risk Ratio (M‐H, Random, 95% CI)	3.12 [1.87, 5.21]
4.2 Gastrointestinal side effects	2	132	Risk Ratio (M‐H, Random, 95% CI)	8.23 [0.90, 75.11]
4.3 Neurological side effects	2	132	Risk Ratio (M‐H, Random, 95% CI)	13.10 [1.43, 120.05]
4.4 Infection (total)	2	86	Risk Ratio (M‐H, Random, 95% CI)	1.53 [0.69, 3.40]
4.5 CMV infection (total)	2	132	Risk Ratio (M‐H, Random, 95% CI)	2.25 [0.31, 16.08]
4.6 Malignancy (total)	2	132	Risk Ratio (M‐H, Random, 95% CI)	0.26 [0.03, 2.30]

Comparison 3. Treatment of first rejection (T cell): muromonab‐CD3 versus other antibody (stratified by comparator)

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Comparison 4. Treatment of first rejection (B cell): rituximab + steroids versus steroids alone

Outcome or subgroup title	No. of studies	No. of participants	Statistical method	Effect size
1 Failure of reversal of acute rejection Show forest plot	2	53	Risk Ratio (M‐H, Random, 95% CI)	0.94 [0.54, 1.64]

2 Additional treatment required Show forest plot	1	20	Risk Ratio (M‐H, Random, 95% CI)	1.33 [0.40, 4.49]

3 Graft loss or death with a functioning graft within 12 months Show forest plot	2	58	Risk Ratio (M‐H, Random, 95% CI)	1.0 [0.23, 4.35]

4 Death within 12 months Show forest plot	2	58	Risk Ratio (M‐H, Random, 95% CI)	0.0 [0.0, 0.0]

5 Treatment adverse events Show forest plot	2		Risk Ratio (M‐H, Random, 95% CI)	Subtotals only

5.1 Fever, chills, malaise after administration	1	15	Risk Ratio (M‐H, Random, 95% CI)	4.91 [0.31, 76.58]
5.2 CMV infection	2	58	Risk Ratio (M‐H, Random, 95% CI)	0.93 [0.11, 8.04]
5.3 UTI/pyelonephritis	1	38	Risk Ratio (M‐H, Random, 95% CI)	5.73 [1.80, 18.21]
5.4 Sepsis	1	38	Risk Ratio (M‐H, Random, 95% CI)	11.67 [0.60, 225.17]
5.5 BK virus infection	1	38	Risk Ratio (M‐H, Random, 95% CI)	0.47 [0.02, 9.01]
5.6 HSV infection	1	38	Risk Ratio (M‐H, Random, 95% CI)	7.00 [0.31, 159.85]
5.7 Nocardia infection	1	38	Risk Ratio (M‐H, Random, 95% CI)	0.78 [0.03, 17.76]
5.8 Gastrointestinal disorders	1	38	Risk Ratio (M‐H, Random, 95% CI)	0.49 [0.06, 3.74]
5.9 Blood and lymphatic system disorders	1	38	Risk Ratio (M‐H, Random, 95% CI)	0.82 [0.10, 7.04]
5.10 Neoplasm	1	38	Risk Ratio (M‐H, Random, 95% CI)	0.78 [0.03, 17.76]
5.11 Other/unspecified	1	38	Risk Ratio (M‐H, Random, 95% CI)	0.21 [0.01, 3.54]

Comparison 4. Treatment of first rejection (B cell): rituximab + steroids versus steroids alone

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Comparison 5. Treatment of steroid‐resistant rejection: antibody versus other antibody (stratified by antibody type)

Outcome or subgroup title	No. of studies	No. of participants	Statistical method	Effect size
1 Failure of acute rejection reversal Show forest plot	5	244	Risk Ratio (M‐H, Random, 95% CI)	1.07 [0.63, 1.81]

1.1 Muromonab‐CD3 versus ATG	3	173	Risk Ratio (M‐H, Random, 95% CI)	1.00 [0.17, 5.76]
1.2 Muromonab‐CD3 versus ALG	2	71	Risk Ratio (M‐H, Random, 95% CI)	1.12 [0.78, 1.60]
2 Additional treatment required Show forest plot	1		Risk Ratio (M‐H, Random, 95% CI)	Subtotals only

2.1 Muromonab‐CD3 versus ATG	1	55	Risk Ratio (M‐H, Random, 95% CI)	1.16 [0.40, 3.35]
3 Recurrent rejection Show forest plot	5	284	Risk Ratio (M‐H, Random, 95% CI)	0.78 [0.47, 1.28]

3.1 Muromonab‐CD3 versus ATG	3	174	Risk Ratio (M‐H, Random, 95% CI)	1.08 [0.71, 1.64]
3.2 Muromonab‐CD3 versus ALG	2	110	Risk Ratio (M‐H, Random, 95% CI)	0.47 [0.21, 1.06]
4 Graft loss censored for death (< 1 year) Show forest plot	5	244	Risk Ratio (M‐H, Random, 95% CI)	0.86 [0.34, 2.17]

4.1 Muromonab‐CD3 versus ATG	3	173	Risk Ratio (M‐H, Random, 95% CI)	1.54 [0.28, 8.57]
4.2 Muromonab‐CD3 versus ALG	2	71	Risk Ratio (M‐H, Random, 95% CI)	0.59 [0.24, 1.49]
5 Graft loss or death with a functioning graft (< 1 year) Show forest plot	5	211	Risk Ratio (M‐H, Random, 95% CI)	0.81 [0.43, 1.51]

5.1 Muromonab‐CD3 versus ATG	4	190	Risk Ratio (M‐H, Random, 95% CI)	0.87 [0.49, 1.55]
5.2 Muromonab‐CD3 versus ALG	1	21	Risk Ratio (M‐H, Random, 95% CI)	0.13 [0.01, 2.26]
6 Death within 12 months Show forest plot	3	175	Risk Ratio (M‐H, Random, 95% CI)	0.39 [0.09, 1.65]

6.1 Muromonab‐CD3 versus ATG	2	115	Risk Ratio (M‐H, Random, 95% CI)	0.41 [0.08, 2.05]
6.2 Muromonab‐CD3 versus ALG	1	60	Risk Ratio (M‐H, Random, 95% CI)	0.33 [0.01, 7.87]
7 Treatment adverse events Show forest plot	5		Risk Ratio (M‐H, Random, 95% CI)	Subtotals only

7.1 Fever, chills, malaise after administration	3	140	Risk Ratio (M‐H, Random, 95% CI)	2.54 [0.18, 34.92]
7.2 Infection (bacterial)	2	109	Risk Ratio (M‐H, Random, 95% CI)	8.64 [1.64, 45.56]
7.3 Infection (viral)	1	59	Risk Ratio (M‐H, Random, 95% CI)	0.53 [0.29, 0.97]
7.4 Infection (fungal)	1	50	Risk Ratio (M‐H, Random, 95% CI)	7.56 [0.41, 139.17]
7.5 CMV infection	5	284	Risk Ratio (M‐H, Random, 95% CI)	0.93 [0.60, 1.43]
7.6 Malignancy (total)	2	115	Risk Ratio (M‐H, Random, 95% CI)	2.09 [0.28, 15.66]
8 Serum creatinine post treatment (3 days) Show forest plot	1	38	Mean Difference (IV, Random, 95% CI)	1.50 [‐0.25, 3.25]

9 Serum creatinine at 12 months Show forest plot	4		Mean Difference (IV, Random, 95% CI)	Subtotals only

9.1 Muromonab‐CD3 versus ATG	4	179	Mean Difference (IV, Random, 95% CI)	5.93 [‐18.46, 30.32]

Comparison 5. Treatment of steroid‐resistant rejection: antibody versus other antibody (stratified by antibody type)

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