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Surgical EndoscopyAnd Other Interventional TechniquesOfficial Journal of the Society ofAmerican Gastrointestinal andEndoscopic Surgeons (SAGES) andEuropean Association for EndoscopicSurgery (EAES) ISSN 0930-2794 Surg EndoscDOI 10.1007/s00464-014-4045-1

Donor safety in live donor laparoscopicliver procurement: systematic review andmeta-analysis

Mohamed Bekheit, Philipe-AbrahimKhafagy, Petru Bucur, Khaled Katri,Ahmed Elgendi, Wael Nabil Abdel-salam, Eric Vibert, et al.

1 23

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REVIEW

Donor safety in live donor laparoscopic liver procurement:systematic review and meta-analysis

Mohamed Bekheit • Philipe-Abrahim Khafagy •

Petru Bucur • Khaled Katri • Ahmed Elgendi •

Wael Nabil Abdel-salam • Eric Vibert • El-said El-kayal

Received: 12 September 2014 / Accepted: 11 December 2014

� Springer Science+Business Media New York 2014

Abstract

Background Donor safety is a major concern in live

organ donation. Live donor laparoscopic liver procurement

is an advanced surgical procedure that is performed in

highly specialized centers. Since its first report, not much

progress has been endeavored for that procedure.

Methods We planned to include all the randomized and

comparative nonrandomized studies. Patients’ population:

live donors who are submitted to organ procurement via

laparoscopy.

Results Out of 5,636 records retrieved from the literature,

only seven nonrandomized studies were included in this

review, which encompassed 418 patients, 151 patients of

whom underwent laparoscopic procurement. The quality

scores for the included studies ranged from 66 to 76 %.

The operative time was significantly shorter in the con-

ventional open group (SD = 0.863, 95 % CI 0.107–1.819).

Blood loss in the laparoscopic group was comparable with

the conventional open approach (SD = -0.307, 95 % CI

-0.807 to 0.192). In subgroup analysis, laparoscopy was

protective against blood loss in laparoscopic parenchymal

dissection (SD = -1.168, 95 % CI -1.758 to -0.577).

The hospital stay was equal in both groups. Patients in

laparoscopic group consumed fewer analgesics compared

with conventional open group (SD = -0.33, 95 % CI

-0.63 to -0.03). Analgesics use was lower in the laparo-

scopic group compared with the conventional approach.

The rate of Clavien complications was equal in both groups

(OR 0.721, 95 % CI 0.303–1.716). No difference was

found between subgroup analysis based on the harvested

liver lobe. Funnel plot and statistical methods used

revealed low probability of publication BIAS.

Conclusions Live donor laparoscopic liver procurement

could be as safe as the conventional open approach. Lower

blood loss and lower consumtion of analgesics might be

offered in the laparoscopic approach.

Keywords Abdominal � Digestive � Hepatobiliare

(liver) � Transplantation � Surgical � Laparoscopic � Live

donor � Liver transplantation

Live organ donation is a noble human gesture that should be

rewarded with much respect. Maintaining the highest pos-

sible level of donation safety is the least that could be done in

return. Live donation is increasingly becoming a corner stone

in organ transplantation, encountering the frustrating organ

shortage from cadaveric donation [1]. Donor safety is of

great concern in living donation [2], therefore the medical

reward of this noble act is to minimize the donors‘ sacrifice.

In live liver donation, the conventional approach with large

M. Bekheit

Minimal Invasive Surgery Unit, Department of Surgery, El

Kabbary General Hospital, El Kabbary, Alexandria, Egypt

M. Bekheit (&)

CIRE Plateform, INRA Centre Val de Loire, 37380 Nouzilly,

France

e-mail: [email protected];

[email protected]

M. Bekheit � P. Bucur � E. Vibert

INSERM, Unit 785, Centre Hepatobiliaire, Paul Brousse

Hospital, 94804 Villejuif, France

P.-A. Khafagy

Department of Radiology, Le Raincy-Montfermeil Hospital,

93370 Monfermeil, France

K. Katri � A. Elgendi � W. N. Abdel-salam � E. El-kayal

HPB Surgery Unit, Department of Surgery, Faculty of Medicine,

Alexandria Main University Hospitals, Alexandria University,

Alexandria, Egypt

123

Surg Endosc

DOI 10.1007/s00464-014-4045-1

and Other Interventional Techniques

Author's personal copy

variable subcostal incision is considered the standard pro-

cedure [3]. Nonetheless, this approach is associated with a

relatively high morbidity rate reaching up to 40 % in some

series [4]. Noteworthy, the large wound incurred during the

procedure and its related morbidities that, despite being

usually indolent, yet are manifest and cumbersome to most of

the donors who are usually young fit adults. Even without

complications, the incision itself is sufficiently disturbing in

appearance for most of the donors [5].

Minimal invasive surgery has developed significantly

over the past few decades. Laparoscopic surgery has pro-

ven to encompass numerous privileges in terms of post-

operative recovery and wound-related complications as

well as intraoperative events such as blood loss. Laparo-

scopic liver surgery is a well-recognized and -practiced

procedure in many centers all over the world. Since its first

report in 2002 [6], laparoscopic live donor hepatectomy

had a much slower spread than other laparoscopic proce-

dures. Nonetheless, it is performed frequently in limited

practice settings among particularly specialized centers.

Indeed, from the cosmetic point of view, live laparoscopic

liver procurement is constrained by the necessity to retrieve

an intact, minimally traumatized organ. Up to this moment,

it is not known systematically whether this approach offers

advantages over the conventional open approach.

Hypothesis We hypothesize that live donor laparoscopic

liver procurement is as safe as conventional open pro-

curement (Ho).

Aim

The objective of this study is to determine the safety profile

of laparoscopic procurement compared with the conven-

tional open procurement in live liver donors.

Objective

The objective is to identify all comparative trials compar-

ing the laparoscopic liver procurement with the conven-

tional open procurement, to assess the quality of those

trials; to determine the total number of patients included in

comparative trials and their characteristics; and to identify

the reported complications and other factors representing

the safety of the procedure such as operative time, blood

loss, consumption of analgesics, and hospital stay.

Methodology

Study inclusion in the review is based on the patient,

intervention, comparison, outcome (PICO) criteria.

Study population

The study included live donors who are submitted to organ

procurement via laparoscopy.

Types of intervention and comparison

Studies comparing the laparoscopic procurement to the

conventional open procurement will be considered for

inclusion. Laparoscopic procedures will be considered if it

is one of the following types: pure laparoscopic surgery in

which the whole procedure including the parenchymal

transaction has been performed in the laparoscopic

approach; laparoscopic-assisted surgery in which laparo-

scopic approach is used for dissection of the fibrous

attachment of the liver; or hand-assisted surgery where a

hand port is used during ligament dissection phase and/or

parenchymal dissection phase.

Outcome measures

The primary outcome measure is the Clavien scores [7] for

donor complications after procedures of live donation.

Secondary outcomes included items that would repre-

sent the hospital stay and the operative time as well as the

post-operative consumtion of analgesics.

Data transformation: all reported complications will be

transformed to the corresponding grade of Clavien score.

For the studies reporting Clavien scoring, the scores will be

treated as they are.

Typs of studies

The first target is seeking for randomized controlled trials

comparing both approaches. Other types of comparative

studies will also be considered for inclusion.

Search strategy

We plan to search Pubmed, Ovid (embase, medline), web

of science, trip database, and Cochrane database. We also

plan to do cross-references checking of the included stud-

ies, looking for related citations. We plan to have no

restriction on inclusion due to language of publication,

since the authors’ team is capable of handling more than

four live languages. Furthermore, we plan to seek profes-

sional translation for other languages provided that the title

and abstract are available in one of the languages known to

the authors to identify eligibility for inclusion. The sum-

mary of search strategy and search terms is presented in

Table 1.

We do not plan to manually search the archives. We also

do not plan to seek authors for unpublished data.

Surg Endosc

123


Study selection and data extraction

The first author (MB) was responsible for conducting the

databases’ search and retrieval of full text studies. The first

(MB) and the second (P-A. K) authors were responsible for

studies’ selection and to list excluded studies with reasons

for exclusion. We plan to seek a senior author’s opinion to

resolve any conflict if any regarding studies’ inclusion and

quality scoring.

MB and PA.K plan to extract the following data:

1. Inclusion and exclusion criteria

2. Year of publication

3. Sample size

4. Demographics of study population (age, gender, BMI)

5. Intervention’s description

6. Outcome data: (Analgesic use, Blood loss, hospital

stay, donor complications, and grading {Clavien I, II,

III, IV}

7. Methodological quality assessment

Assessment of methodological quality

We plan to assess the methodological quality of the trials

without masking the trial names. We plan to follow the

instructions given in the Cochrane handbook of systematic

reviews of interventions [8]. We plan to evaluate the reported

randomization and the process of reporting complications

since there is risk of bias associated with overestimation of

intervention effects [9–12] as detailed in Appendix 1.

Inclusion and exclusion after quality assessment

The purpose of the quality assessment task is to identify the

level of evidence, on which conclusions will be based.

Nonetheless, we plan to include all randomized trials as

well as all comparative nonrandomized trials.

Exclusion criteria will include

• Single-arm studies

• Studies with significantly incomplete outcome data

• Studies comparing with nonstandard open procedure or

with an outside protocol laparoscopic intervention.

Data synthesis and statistical methods

Raw data on complications will be converted to Clavien

scoring, while in the case of studies reporting the compli-

cations grading only, the grading will be extracted as it is.

Analysis of each grade complication frequency will be

conducted separately, and then a pooled frequency estimate

will be calculated. We plan to perform the meta-analyses as

close as possible to the recommendations of the Cochrane

Collaboration [8] using the software Comprehensive met

analysis (Biostat. Inc. USA) for the statistical analysis, and

QIQQA research management software (QiqqaTM, Quan-

tisle Ltd. London, UK) for the annotation report produc-

tion. For dichotomous variables, we plan to calculate odds

ratio and the log odds ratio with standard error for

dichotomous and categorical data. For continuous vari-

ables, we plan to calculate the standardized differences of

means with standard error. We elect to calculate the

‘‘Hedges’s g’’ and its standard error for both types of data

to represent the overall (pooled) effect estimate when

including all the parameters expressing donor safety. For

data describing central tendency in median and range

instead of mean and standard deviation, we intend to

convert these values into mean and standard deviation,

when necessary, using the methods suggested by Hozo

et al. [13].

Table 1 Details of the search strategy and the accessed databases based on search terms

Database Period Search terms

Pubmed March 2014/updated May

2014

Laparoscopic live donor hepatectomy

Updated-laparoscopic live donor hepatectomy, ‘‘Laparoscopy* AND liver transplantation’’,

‘‘Laparoscopy AND liver donor’’, ‘‘Laparoscopy AND liver transplantation’’

Embase April 2014 Laparoscopic live donor hepatectomy

Midline April 2014 Laparoscopic live donor hepatectomy

Ovid April 2014 Laparoscopic live donor hepatectomy

Trip database May 2014 Laparoscopic live donor hepatectomy

Web of science March 2014/updated May

2014

Laparoscopic live donor hepatectomy

Updated term: ‘‘laparoscopic live donor hepatectomy’’, ‘‘Laparoscop* AND liver

transplantation’’, ‘‘Laparoscopy AND liver donor’’, ‘‘Laparoscopy AND liver transplantation’’

‘‘Laparoscop*AND liver AND Transplant*

Cochrane

database

May 2014 Laparoscopic live donor hepatectomy

*It is used to include the different sufixes to the term root

Surg Endosc

123


For outcomes such as odds ratio for death, we plan to

use generic inverse variance method for the meta-analysis.

We plan to use a random-effect model [14] and a fixed-

effect model [15]. In case of discrepancy between the two

models, we plan to explore heterogeneity by Chi squared

distribution test (Q test) with significance set at p value of

0.10, and to report the random-effect model in case of

significant Q test. We plan to measure the quantity of

heterogeneity by I2 [16]. We considered an I2 of 30 % or

more to represent heterogeneity.

We plan to perform the analysis on an intention-to-treat

basis [17] for patients who underwent conversion from

laparoscopic to open approach; whenever possible. For that

purpose, multiple imputation analysis will be conducted on

SPSS version 20 (IBM Inc. Chicago, IL, USA). Otherwise,

we plan to adopt the ‘available case analysis.’ In case we

found ‘zero-event’ trials in statistically significant out-

comes, we plan to perform a sensitivity analysis with and/

or without empirical continuity correction factors as sug-

gested by Sweeting et al. [18]: one-study removed tech-

nique, and both-models compared technique. We decided

to conduct sensitivity analysis for outcomes that showed

heterogeneity in the fixed-effect model. We examined the

difference in assumption based on the model between

random- and fixed-effect models, and we conducted one-

study removed technique to test the sensitivity. Whenever

the two models are in concordance, we consider the

assumption as correct.

Subgroup analysis

We plan to conduct the following subgroup comparisons:

• Studies on right lobe versus those on left lateral section

• Studies with laparoscopic parenchymal dissection ver-

sus open parenchymal dissection

Meta-regression

Exploiting the total quality score against the pooled effect

size of the complications will be conducted according to

the unrestricted maximum likelihood model. This is par-

ticularly important since we decided to include randomized

and nonrandomized studies in the review.

Bias exploration

We plan to use a funnel plot to explore bias [19, 20] based

on standard error on the vertical axis as recommended by

Sterne et al. [21]. We also plan to perform linear regression

described by Egger et al. to determine the funnel plot

asymmetry [20].

Results

The PRISMA flow chart (Fig. 1) summarizes the search

findings. No randomized controlled trials were identified in

the identified records. Out of the nine eligible comparative

studies, seven were included in the quantitative data syn-

thesis. The included studies encompassed 419 patients, of

whom 150 patients, who underwent laparoscopic procure-

ment approach, were compared with 269 patients who

underwent the conventional open approach. 42 donors

underwent open left lateral section procurement, and 41

donated laparoscopically. 79 donated the entire left lobe in

the conventional open approach, while 31 donated under

laparoscopy. For the right lobe, 148 donors donated in the

conventional open approach and 78 donors donated under

laparoscopy.

The baseline demographic criteria (age, gender distri-

bution, and BMI) were similar between the laparoscopic

and the conventional approaches. Tables 2 and 3 summa-

rize the characteristics of the included studies and the

extracted data of interest from each study.

Methodological quality of the analyzed studies

We were not able to identify any randomized trials for the

review. Furthermore, all of the included studies scored

between 60 and 76 % on the quality score adapted from

[28]. Table 4 summarizes the quality score items and the

scores of the included studies. We provide a list of

excluded studies after initial eligibility [6, 29–61].

Assessment of baseline characteristics

between the compared groups in the included studies

There was no heterogeneity among the included studies

reporting on age (Q = 8.25, df = 6, p = 0.22, I2 = 27 %).

In the fixed-effect model, the age among the laparoscopic

group was lower than that in the conventional group (SD

difference in means = -0.344, 95 % CI -0.555 to

-0.133). Unlike the reported BMI, there was no hetero-

geneity among the included studies (Q = 10.2, df = 4,

p = 0.03, I2 = 60 %). In the random-effect model, there

was no difference between the groups (SD difference in

means = -0.15, 95 % CI -0.526 to 0.224). Similarly,

there was difference in the gender distribution between the

groups [point estimate (OR) = 0.7, 95 % CI 0.42–1.2] as

was revealed by the fixed-effect model (Q = 8.5, df = 6,

p = 0.2, I2 = 29 %). These baseline characteristics are

summarized in Fig. 2. In subgroup analysis based on the

procured lobe, 82 donors were included for left lateral

section procurement (41 in laparoscopy), while 222 right

lobe donations (98 in laparoscopy) were included. The

donor’s‘ age was significantly lower in the left lateral

Surg Endosc

123


section in a fixed-effect model (SD diff in means =

-0.623, p = 0.006), unlike the right lobe where there was

no age difference. BMI was as well lower in the laparo-

scopic left lateral group (SD diff in means = -0.9,

p = 0.015), while no difference in the BMI was observed

in the right lobe subgroup.

Outcome items

Operative time

There was significant heterogeneity among the included

studies regarding the operative: (Q = 48, df = 6, p \ 0.001)

for the fixed-effect model. Still applying the random-effect

model shows significantly shorter operative time for the

conventional open approach compared with laparoscopic

approaches (SD difference in means = 0.552, 95 % CI

0.011–1.084) for the pooled effect estimate from the

included studies.

Subgroup analysis based on the approaches for paren-

chymal dissection demonstrates that in case of the laparo-

scopic dissection for left lateral sectionectomy (Q = 1.7,

df = 1, p = 0.2), the operative time was significantly

shorter than that for the open approach (standardized dif-

ference of mean = 0.863, 95 % CI 0.107–1.819). For

studies using open approach for parenchymal dissection

Fig. 1 PRISMA chart

illustrating the search strategy,

excluded records, and the

records included in quantitative

analysis. a Includes case reports,

series, technical descriptions.b Excluded after discussion

between the first and second

reviewers

Table 2 Summary of characteristics of the included studies

Study (year) Hand assisted

versus only

laparoscopic

Parenchymal

dissection

(open or lap)

Lobe Incision Sampling Temporal Quality

score (%)

Zhang (2014) [3] Hand Open Right Midline Case matched Prospective 76

Kim (2011) [23] Pure Laparoscopic Left lateral Pfennenstiel Nested case

control

Retrospective 66

Baker (2009) [24] Hand Open Right Midline Case control Retrospective 75

Soubrane (2006) [25] Pure Laparoscopic Left lateral Pfennenstiel Nested case

control

Retrospective 68

Thenappan (2011) [26] Hand Open Left lateral Midline Nested case

control

Retrospective 68

Choi (2012) [27] Laparoscopic Open Right Right subcostal Nested case

control

Retrospective 67

Marubashi (2013) [28] Hand Open Left lobe?/left lateral Midline Nested case

control

Retrospective 71

Surg Endosc

123


(laparoscopy was used only for dissection of attachments)

(Q = 48, df = 4, p \ 0.001, I2 = 90 %), the mixed-effect

model demonstrated that using laparoscopy only for

hepatic mobilization resulted in no difference in operative

time compared with groups having the conventional open

approach for procurement (Fig. 3).

Sensitivity analysis (comparing both models technique)

of the assumption of the model on the operative time

demonstrated that both models fixed ( p = 0.001) and

random (p = 0.046) are significant in the same direction

(shorter operative time for the conventional approach).

Subgroup analysis based on the procured lobe identified

no significant difference in operative time between the the

conventional and laparoscopic groups in both right and left

lateral subgroup resections in the random-effect model The

model was selected based on the heterogeneity test

(Q = 6.3, p = 0.04, I2 = 69 % for the left lateral and

Q = 38, p \ 0.001, I2 = 94 %).

Blood loss


studies (Q = 30.6, df = 6, p \ 0.001, I2 = 80.39 %). The

random-effect model showed insignificant difference in the

blood loss between the laparoscopic and the conventional

approaches (SD difference in means = -0.307, 95 % CI

-0.807 to 0.192).

Subgroup analysis

The included studies demonstrated heterogeneity of the effect

estimate of blood loss (Q = 30.6, df = 6, p\0.001,

I2 = 80.39 %). The overall mixed-effect model demonstrated

that the blood loss was significantly lower in the laparoscopic

approaches versus the conventional approach (Standardized

difference in means = -0.509, 95 % CI -0.89 to -0.13). In

subgroup analysis based on the approach of parenchymal

dissection, laparoscopic parenchymal dissection, which was

performed for left lateral section procurement, was more

protective against blood loss compared with the conventional

open approach (SD difference in means = -1.168, 95 % CI

-1.758 to -0.577). When laparoscopy was used only for

hepatic mobilization, blood loss was equal in both arms of

comparison (Fig. 4). Furthermore, there were no significant

differences in the blood loss between the conventional and

laparoscopic groups for both the left lateral section and the

right lobe (Q = 8.2, p = 0.017, I2 = 75.5 % and Q = 16.6,

p\0.001, I2 = 87.9).

Table 3 Summary of the measurements of interest in the included studies

Study (year) Gender

(male)

n/total

Age (years)

mean (SD)

BMI (kg/m2)

Mean (SD)

Blood loss (ml)

mean (SD)

Operative (min)

mean (SD)

Analgesia (days)

mean (SD)

Hospital (days)

mean (SD)

Zhang (2014) [3]

Lap 13/25 37.2 (8.7) 23.8 (2.6) 378 (112) 385.9 (47) 2.4 (1) 7 (1.4)

Open 14/25 37.4 (10.5) 22.6 (3) 423 (139) 378 (59) 3.2 (1) 8.7 (2.4)

Kim (2011) [23]

Lap 1/11 29 (6) 396 (72) 330 (68) 6.9 (0.3)

Open 6/11 35 (2) 464 (78) 306 (29) 9.8 (0.9)

Baker (2009) [24]

Lap 15/33 37 (10.3) 25.8 (4) 417 (217) 265 (48) 4.3

Open 13/33 39 (11) 25.9 (4.3) 550 (305) 316 (61) 3.9

Soubrane (2006) [25]

Lap 2/16 29 (5) 23.8 (1.6) 18.7 (44.2) 320 (67) 2 (0.9)

Open 1/14 32 (5) 24.9 (0.1) 199.2 (185.4) 244 (55) 2.2 (0.9)

Thenappan (2011) [26]

Lap 7/15 33.9 (8.9) 814 (720) 312 (67.8) 1.6 (0.97) 6 (2)

Open 6/15 35.7 (8) 733 (457) 324 (105.6) 2 (1.4) 6 (3.7)

Choi (2012) [27]

Lap 12/20 29.7 (10) 23.6 (2.8) 870 (653) 383.6 (41.7) 2.5 (1.1) 12 (2.8)

Open 58/90 36.8 (12) 23.6 (2.9) 531 (322.6) 303 (61.5) 2.55 (1.1) 12 (3.6)

Marubashi (2013) [28]

Lap 13/31 35.8 (8.4) 21.3 (3.6) 353 (396) 435 (103) 10.3 (3.3)

Open 54/79 37.8 (10) 22.6 (3) 456 (347) 383 (73) 18.3 (16.7)

Surg Endosc

123


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Surg Endosc

123


Analgesic use

Only four studies reported information on the post-opera-

tive consumption of analgesics. There was no

heterogeneity among the included studies (Q = 3.9,

df = 3, p = 0.25, I2 = 24 %). The overall fixed-effect

model showed significantly fewer analgesics use among

patients who underwent laparoscopic approach (SD

Fig. 2 Forest plots of the base line characteristics (A age years, B BMI kg/m2, C male gender frequency) of the included studies’ population

Surg Endosc

123


difference in means = -0.33, 95 % CI -0.63 to -0.03).

This was particularly pronounced among the subgroups

who had open parenchymal dissection through midline

incision (SD difference in means = -0.618, 95 % CI

-1.068 to -0.168) (Fig. 5).

Hospital stay


studies (Q = 38.7, df = 6, p \ 0.001, I2 = 84.5 %). In the

random-effect model: the hospital stay was equal in the

laparoscopic group compared with the conventional one

(SD difference in means = -0.577, 95 % CI -1.158 to

0.004). Nonetheless, for the fixed-effect model, the hospital

stay was shorter in the laparoscopic group (p = 0.003). In

sensitivity analysis, we removed one study (the lowest

quality score), but both models retained their values. So we

resort to subgroup analysis.

For the subgroup analysis, in the overall mixed-effect

model (SDM = -0.272, 95 % CI -0.674 to 0.130), the

hospital stay was equal for both the laparoscopic and the

conventional groups. In the subgroup analysis based on the

approach of parenchymal dissection, both subgroups (open

parenchymal dissection and laparoscopic parenchymal

dissection) of the laparoscopic approaches resulted in equal

hospital stay compared with the conventional approach

(Fig. 6). Subgroup analysis based on the procured lobe

demonstrated no significant difference in hospital stay

between the laparoscopic and the conventional groups in

the left lateral section and right lobe subgroups in the

Fig. 3 Forest plot for the estimate of the operative time comparing the laparoscopic approaches versus conventional. The operative time was

shorter in the open group. It also demonstrated the longer operative time in the subgroup where laparoscopy was used for parenchymal dissection

Fig. 4 Forest plot with group analysis demonstrating the lower

estimate of blood loss in the subgroup where laparoscopy was used

for parenchymal dissection in left lateral section procurement and the

no difference in the subgroup where laparoscopy was used only for

hepatic mobilization

Surg Endosc

123


random-effect model (Q = 25.5, p \ 0.001, I2 = 92 %

and Q = 8.9, p = 0.01, I2 = 77.7 % for left and right,

respectively).

Complications

Clavien grade I complication There was no significant

heterogeneity among the included studies (Q = 5.856,

df = 6, p = 0.4). In the fixed-effect model (OR 0.837,

95 % CI 0.431–1.628), both the conventional and the lap-

aroscopic approaches had the same risk factor for grade

Clavien I complication. The frequency of grade one com-

plication among the laparoscopic group was 16 events for

the 151 patients included in this review compared with 32

events among the 267 patients who underwent the con-

ventional open approach. There was no difference in the

estimate in the subgroup analysis based on the approach for

parenchymal dissection (Fig. 7A). No difference was seen

in Clavien grade I complications in subgroup analysis

based on procured lobe (OR 0.4, p = 0.2 and OR 1.2,

p = 0.7) for left lateral and right lobes.

Clavien grade II complications: Only six studies reported

on Clavien II complications. There was no heterogeneity

among the included studies (Q = 1.1, df = 5, p = 0.9,

I2 = 0 %). In the fixed-effect model, the rate of Clavien II

grade complication was similar in the laparoscopic 6/151

versus 22/267 to that in the conventional open approach

group (OR 0.505, 95 % CI 0.190–1.343). This was also

similar when the laparoscopy was used only for hepatic

mobilization or for parenchymal dissection as well

(Fig. 7B). Also, the rate of this grade was similar between the

Fig. 5 Forest plot for subgroup analysis based on the incision site showing the lower estimate of consumption of analgesics among subgroup of

patients who underwent laparoscopic hepatic mobilization and open parenchymal dissection through midline incision

Fig. 6 Forest plot for group comparison, showing no difference in the overall estimates of hospital stay in both groups

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123


conventional and the laparoscopic groups in a subgroup

analysis of the procured lobe (OR 0.45, p = 0.3 and OR 0.49,

p = 0.27 for left lateral section and right lobe, respectively).

Clavien grade III complications Two studies reported on

Clavien III complications. There was significant hetero-

geneity between the included studies in terms of

(Q = 3.13, df = 1, p = 0.007, I2 = 68 %). In the mixed-

effect model, the incidence rates of grade III complications

were equal when compared: 3/151 in the laparoscopic

group versus 9/267 in the conventional approach group

(OR 1.989, 95 % CI 0.087–45.49). The subgroup analysis

demonstrated that all Clavien III occurred when the lapa-

roscopy is used only for hepatic mobilization. In one-study

removed sensitivity analysis technique, the model

assumption was retained (Fig. 7C). Only one study was

included in the subgroup analysis based on the procured

lobe which demonstrated insignificant difference in the

rates of Clavien III (OR 13.9, p = 0.1).

Clavien IV No clavien VI complications were reported in

any of the included studies.

Pooled estimate of combined Clavien complica-

tions There was no heterogeneity among the included

studies when estimating the combined Clavien rates

(Q = 1.799, df = 6, p = 0.9, I2 = 0). The overall fixed-

effect model showed no difference in the incidence rates of

complications between laparoscopic group and the con-

ventional approach group (OR 0.721, 95 % CI

0.303–1.716). Similarly in analysis of the subgroups, there

was no difference in rates between open or laparoscopic

groups whether laparoscopy was used only for hepatic

mobilization or for parenchymal dissection as well

(Fig. 7D). No difference was calculated for the pooled

complication rates based on the procured lobe subgroup

analysis (OR 0.53, p = 0.44 and OR 0.89, p = 0.85 for left

lateral section and right lobe, respectively).

Pooled effect size of the outcomes representing the donor

safety

There was no heterogeneity among the included studies

when assessing the pooled effect estimate for criteria cor-

responding to donor safety (Q = 5.52, df = 6, p = 0.47,

I2 = 0). In the fixed-effect model, the different approaches

had the nearly the same outcome (Hedges’s g = -0.236,

95 % CI -0.578 to 0.107). The result was also the same for

the subgroup analysis based on the approach used for

parenchymal dissection (Fig. 8). No difference was

observed for a subgroup analysis based on the procured lobe

(Hedges’ g = -0.43, p = 0.17 and Hedges’ g = -0.13,

p = 0.55 for left lateral section and right lobe, respectively).

BIAS exploration was conducted for selected outcome

variables using funnel plots with regression intercept test,

trim and fill method, and Kendall‘s rank correction. For the

operative time, studies showed symmetric distribution

around the common standardized difference in means (Fig.

9A). This was confirmed by the Egger’s regression inter-

cept [Intercept = 0.55, 95 % CI -12.6 to 13.7, p (1-

tail) = 0.4, (2-tail) = 0.9]. Kendall’s Tau without conti-

nuity correction was s = 0.04, p = 0.8, while with conti-

nuity correction was s = 0, p = 1.

Similarly, the Egger’s regression intercept for blood loss

demonstrated statistical symmetry [intercept = -3.47,

95 % CI -12.4 to 5.5, p (1-tail) = 0.18, (2-tail) = 0.36].

The Kendall’s Tau without continuity correction was

s = -0.3, p = 0.2, while with continuity, the correction

was s = -0.2, p = 0.36. In trim and fill methods, only two

studies were required to nullify the effect (Fig. 9B).

The Egger’s regression intercept test demonstrated sym-

metry of the plots for the pooled estimates of combined Clavien

complications [intercept = -0.59, 95 % CI -3.45 to 2.27,

p (2-tail) = 0.6, (1-tail) = 0.3]. The Kendall’s Tau without

continuity correction was s = -0.14, p = 0.6, and with con-

tinuity, correction was s = -0.09, p = 0.7 (Fig. 9C).

Meta-regression was performed using the total quality

score as a predictor variable for the pooled effect estimate

of the donor safety criteria considered in this review

(Fig. 10). For the unrestricted maximum likelihood model:

Q = 0.34, df = 1, p = 0.56, s2 = 0.

Discussion

Live donor laparoscopic liver procurement seems to be as

safe as open approach, even when laparoscopy is only used

for hepatic mobilization. It seems that the effect modifi-

cation imposed by the use of laparoscopy in liver pro-

curement demonstrated potential benefits related to the

lower blood loss, particularly in the subgroup where

parenchymal dissection was performed in laparoscopy. The

two studies reported on laparoscopic parenchymal dissec-

tion were for left lateral sectionectomy [22, 24]. The

potential for lower blood loss in pure laparoscopic liver

procurement is similar to what is reported as a difference

between laparoscopic and open liver resection [62]. Per-

haps, the fact that there is a difference in blood loss in left

lateral section harvesting while there is no such difference

in right lobe is related to two important reasons: the first

one is that the left lateral section resection is generally

easier compared with other lobes. The second reason could

be that the parenchymal thickness in the dissection plane is

relatively thinner than any other dissection plane. Fur-

thermore, patients who underwent laparoscopic approaches

generally consumed lower amounts of analgesics than

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123


a

b

c

d

Surg Endosc

123


those who underwent the conventional approach. This

difference was more significant for patients who underwent

laparoscopic hepatic mobilization and midline incision for

parenchymal dissection.

The hospital stay was similar between the comparison

groups, and the rate of complications was similar as well in

both the groups. In the subgroup analysis, all events for

Clavien III grade complications were recorded among the

subgroups, where laparoscopy was used only for liver

mobilization. There was, nevertheless, a tendency of Cla-

vien I complication grade to have lower incidence, but not

significant, in the left lateral section donation under pure

laparoscopic approach. The operative time was generally

longer for the laparoscopic approaches, and this was more

evident in studies that performed the parenchymal dissec-

tion under laparoscopy.

There was no difference in outcome measures in sub-

group analysis based on the procured lobe. Despite this, the

included number of laparoscopic right lobe donations was

higher than that in the left lateral section donations; no

comparative study reported a pure laparoscopic right lobe

donation, and laparoscopy was only used for mobilization

or for hand-assisted surgery. This would highlight that live

donor laparoscopic right liver lobe procurement is still

beyond the core scope of this report.

None among the included studies reported conversion

from laparoscopy to open except the which reported an

intention-to-treat analysis. Complications were reported

among the included studies; therefore, we did not perform

multiple imputations for the intention-to-treat analysis.

None of the included studies reported donor mortality.

In general, donor liver donation is not associated with high

rate of mortality. Trotter et al. reported a donor mortality

rate of 0.15 % after open donation from all the reported

cases in the literature [63]. To our knowledge, the only

confirmed donor death after laparoscopic live donor liver

procurement was the famous Lahey’s clinic case [64].

We were conscious about the liability of sources of

reporting BIAS in this report; that is why we had several

preemptive measures to detect them. We explored publi-

cation BIAS for positive effects (operative time, blood loss,

and hospital stay) as well as for the pooled estimate of the

complications. From the visual inspection of funnel plot,

the distribution of studies around the pooled estimate was

not inhomogeneous. This was confirmed by the statistical

tests used to explore BIAS. Unfortunately, this does not

seem to protect against BIAS, particularly since we just

mentioned none reported donor mortality.

A priori we decided to include non-English language

studies in the review. This decision was less important in

this particular case since we assume the low probability

that such type of studies will be published in other lan-

guage without being published in English. Furthermore,

during our search, we did not come across except one case

report [57]. Despite this, language BIAS is one of the

potential sources of reporting BIAS in this report. This is

still possible as studies from certain locations, even if we

do not have restriction on location, have less access to

publications. We think that this particular sort of BIAS is

less likely for this particular sort of intervention. We did

run cross-references checking of the included studies,

which did not turn out larger number of records.

The other important potential source of BIAS is the

moderate quality of the included studies. Besides that, none

b Fig. 7 A Forest plot for Clavien grade I complication. The frequency

estimates are similar in both groups as well as in subgroup analysis.

B Forest plot for Clavien grade II complication with similar frequency

estimates among the comparisons. C Forest plot for Clavien grade III

comolication with similar frequency estimates among the compari-

sons. D Forest plot for the pooled estimate of combined frequency of

Clavien grades I, II, and III complications, where there is no

difference between the groups

Fig. 8 Forest plot for the pooled estimate from the measured donor safety criteria considered in this review. The model estimates showed similar

safety profiles in both groups as well as in the subgroups

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of the included studies is randomized controlled: all of the

included trials scored between 66 and 76 % on the adapted

quality assessment score for nonrandomized trials. This

highlights the important possibility for sampling BIAS

within the studies. This is particularly a convincing argu-

ment since sampling methodology was one of the low

scored items among the included studies; despite this, there

was no difference in the baseline criteria of the included

Fig. 9 Funnel plot for BIAS

exploration with trim and fill

method for correction.

A Operative time, B blood loss,

C pooled estimate of combined

Clavien grade I, II, and III

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123


participants except for the age that was lower in the lapa-

roscopic group.

We had some modifications on the initially planned

protocol. We updated the search to May–June 2014 in

order not to miss any possible events of the newly pub-

lished trials. This was particularly motivated by the lack of

any randomized trial in the included studies. We also added

one item to the criteria adapted for quality assessment of

nonrandomized trials (intention-to-treat analysis). We jus-

tify this addition to enable us have stratification of the

quality scores that could be reflected as a positive differ-

entiation value in the regression analysis. The one last

modification on the protocol was in the subgroup analysis

based on the incision site, which was not anticipated to be

more suitable for consumption of analgesics.

The beforehand study is the first on the topic it

addresses. Despite the nonexistence of randomized con-

trolled trials on the review topic, we still conducted the

analysis since we decided a priori to synthesize a meta-

analysis from the existing data. This was motivated by our

desire to provide an insight ointon the potential benefits or

harms of the technique, which could be a stepping stone for

further propagation of the technique or a future randomized

trial to be conducted as suggested by Steeves [8]. It is yet

unconceivable that the technique is technically demanding

and it requires highly equipped and experienced facility

and special skill sets that are not currently available for a

large sector of liver surgeons who would require significant

training before embarking on such complex surgery;

therefore, encouragement for further studies to be con-

ducted should be initially restricted to these expert centers.

Conclusions and recommendations

With caution, we accept the null hypothesis, and we would

conclude that the laparoscopic approaches for live donor

liver procurement could be as safe as the conventional open

approach with similar complication rates. Lower blood loss

might be offered in full laparoscopic procurement of left

lateral sectionectomy. Lower consumption of analgesics

was shown among the laparoscopic group. Obviously, the

procedure is still in its infancy, particularly the right lobe

harvesting; despite more than a decade since its first report

has lapsed. There are no robust conclusions that could be

made based on the available data in the literature.

Acknowledgments On the other hand, the authors would like to

acknowledge that access to full text manuscripts was provided via

institutional access of the INSERM; U785, Centre Hepatobiliare, Paul

Brousse Hospital, Villejuif, France.

Disclosures Mohamed Bekheit, Philipe-Abrahim Khafagy, Petru

Bucur, Khaled Katri, Ahmed Elgendi, Wael Nabil Abdel-salam, Eric

Vibert, and El-said El-kayal have no conflict of interest or financial

ties to disclose.

Appendix 1: Methodological assessment of quality

of potential studies to be included in the review

Sequence generation

• Adequate, if the allocation sequence was generated by a

computer or random-number table. Drawing of lots,

tossing of a coin, shuffling of cards, or throwing dice

was considered as adequate if a person who was not

otherwise involved in the recruitment of participants

performed the procedure.

• Unclear, if the trial was described as randomized, but

the method used for the allocation sequence generation

was not described.

• Inadequate, if a system involving dates, names, or

admittance numbers were used for the allocation of

patients.

Allocation concealment

• Adequate, if the allocation of patients involved a cen-

tral independent unit, on-site locked computer, or

sealed envelopes.

• Unclear, if the trial was described as randomized, but

the method used to conceal the allocation was not

described.

• Inadequate, if the allocation sequence was known to the

investigators who assigned participants or if the study

was quasi-randomized. In addition, if there was no

blinding in the trials, the allocation concealment was

considered inadequate if it was possible to predict

future assignments of participants based on previous

assignments such as when fixed size blocks were used

in a single centre trial.

Regression of Quality Score % on Hedges's g

Quality Score %

Hed

ges'

s g

65.00 66.20 67.40 68.60 69.80 71.00 72.20 73.40 74.60 75.80 77.00

0.60

0.34

0.08

-0.18

-0.44

-0.70

-0.96

-1.22

-1.48

-1.74

-2.00

Fig. 10 Meta-regression using the unrestricted maximum likelihood

model using the total quality scores as a predictor variable for pooled

effect estimate of donor safety criteria included in this review

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Blinding

It is not possible to blind the health-care provider (surgeon)

to the group. However, it is possible to blind assessors of

certain outcomes as well as patients to the group. So,

blinding was considered adequate if patients and the out-

come assessors were blinded.

• Adequate, if patients and the outcome assessors were

blinded and the method of blinding was described

provided that the outcome could be blinded from

assessor. However, it is not necessary that for the

patients to be blinded for the outcome to be assessed

without bias (except for one noncrucial outcome;

analgesic use)

• Unclear, if patients and/or the outcome assessors were

blinded and the method of blinding was not described.

• Inadequate, if no attempts were made to blind the

outcome assessors or if the outcome assessors could

easily identify the group to which the patient belongs.

Outcomes assessed with possible blinded assessors

All outcomes considered in the study could be blinded

from assessors except for wound complications.

Incomplete data outcomes

• Adequate, if there were no post-randomization dropouts

or withdrawals or if the post-randomization dropouts

were balanced in both groups or reasons for missing

data unlikely to be related to true outcome(e.g., patients

did not undergo surgery after randomization).

• Unclear, if it is not clear whether there are any dropouts

or withdrawals or if the reasons for these dropouts are

not clear.

• Inadequate, if the reasons for missing data are likely to

be related to true outcomes, ‘‘as-treated’’ analysis was

performed, potentially inappropriate application of

simple imputation, potential for patients with missing

outcomes to induce clinically relevant bias in effect

estimate or effect size.

Selective outcome reporting

• Adequate, if complications were reported or if the trial

protocol was available and the outcome of interest to

this review was reported in the trial protocol.

• Unclear, if there is insufficient information to assess

whether the risk of selective outcome reporting is present.

• Inadequate, if not all the pre-specified outcomes were

reported or if the primary outcomes were changed or if

some of the important outcomes were incompletely

reported.

Other biases: baseline imbalance

• Adequate, if there was no baseline imbalance in

important characteristics.

• Unclear, if the baseline characteristics were not reported.

• Inadequate, if there was a baseline imbalance due to

chance or due to imbalanced exclusion after

randomization.

Each item is given score of 0 (inadequate), 1 (unclear), or 2

(adequate). A maximum score of 12 indicates flawless trial

and a minimum score of 0 indicates inappropriate trial.

We considered any trial classified as adequate sequence

generation, allocation concealment, blinding, incomplete data

outcomes, and selective reporting as trials of low bias-risk.

However, if Clavien IV complications are reported, a trial will

be considered as low bias risk for complications even if

blinding was not performed as long as the trial is classified as

adequate in adequate sequence generation, allocation con-

cealment, incomplete data outcomes, and selective reporting.

Quality assessment of nonrandomized trials

Assessment of quality of nonrandomized trials will be

adapted based on ‘‘systems to rate the strength of scientific

evidence’’ using an adaptation of a subset of the U.S.

preventive task force criteria noted below:

II-2A well-designed prospective cohort with concurrent

control

II-2B well-designed prospective cohort with historic

control

II-2C well-designed retrospective cohort with concurrent

control

II-3 well-designed retrospective case controlled study

Studies will obtain a score based on the sum of point

scoring according to the following criteria, and each cri-

terion will be scored either on a SCALE from 0 (poorest) to

5 (highest) or DICHOTOMOUS (0/1):

A. Clearly focused study question.

B. Clear definition of intervention.

C. Clear definition of primary and secondary outcomes.

D. Sampling of the study population (for nonrandomized

studies):

• 5 = prospective cohort with concurrent control.

• 4 = prospective cohort with historic control.

• 3 = retrospective cohort with concurrent control.

• 2 = retrospective case controlled study.

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• 1 = not specified (N.B: this item takes one since

we will be able to detect the presence of control

group which in any case will rank higher than

single arm studies).

• 0 = case series (will be excluded from the review).

E. Confounders are considered during interpretation of

results through (from 0 to 4 for the method and 1/3 for

each category of confounders)

i. 4 = Restriction in selection.

ii. 3 = Matching on the confounders.

iii. 2 = Demonstrated balanced distribution among

both groups.

iv. 1 = Controlled for in the statistical analysis.

v. 0 = Not done

• List of anticipated potential confounders

(three categories; 1/3 for each):

• Base line and characteristics: age, gender,

BMI

• Anatomical characteristics: lobe

• Experience and learning curve:

F. Statistical methods used to take into account the effect

of multiple variables on the outcome such as regression

analysis, multivariate models.

G. Statistical analysis considered intention to treat princi-

ple for dropouts and switch over (DICHOTOMOUS).

H. Measure of effect of outcome and appropriate measure of

precision (SE, CI) (central tendency and dispersion

measures will be accounted for as sufficient if appropriate).

I. Conclusions supported by results with possible bias

and limitations taken into consideration: i.e.: clinical

significance of effect size provided.

Total score will be provided to the each individual study

with a maximum possible score 41.

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