CURRENT STATUS

Indocyanine Green Fluorescence Angiography and

the Incidence of Anastomotic Leak After Colorectal
Resection for Colorectal Cancer: A Meta-analysis
Renhui Shen, M.D. • Ye Zhang, M.D. • Tong Wang, M.D.
Wuxi People’s Hospital Affiliated to Nanjing Medical University, Wuxi, Jiangsu Province, People’s Republic of China

BACKGROUND:  Anastomotic leak is a life-threatening INTERVENTION:  Indocyanine green was injected

complication of colorectal surgery. Recent studies showed intravenously after the division of the mesentery and
that indocyanine green fluorescence angiography might colon but before anastomosis.
be a method to prevent anastomotic leak. MAIN OUTCOME MEASURES:  The Newcastle–Ottawa
OBJECTIVE:  The purpose of this study was to investigate Scale was used to assess methodologic quality of
whether intraoperative indocyanine green fluorescence the studies. ORs and 95% CIs were used to assess
angiography can reduce the incidence of anastomotic leak. the association between indocyanine green and
anastomotic leak.
DATA SOURCES:  Potential relevant studies were identified
from the following databases: PubMed, Embase, Web RESULTS:  In 4 studies with a total sample size of 1177,
of Science, Cochrane Library, and China National comparing the number of anastomotic leaks in the
Knowledge Infrastructure. indocyanine green and control groups, the ORs were
0.45 (95% CI, 0.18–1.12), 0.30 (95% CI, 0.03–2.98),
STUDY SELECTION:  This meta-analysis included 0.17 (95% CI, 0.01–3.69), and 0.12 (95% CI, 0.03–0.52).
comparative studies investigating the association The combined OR was 0.27 (95% CI, 0.13–0.53). The
between indocyanine green fluorescence angiography difference was statistically significant (p < 0.001), and
and anastomotic leak in patients undergoing there was no significant heterogeneity (p = 0.48; I2 = 0).
surgery for colorectal cancer where the diagnosis
LIMITATIONS:  Data could not be pooled because of
of anastomotic leak was confirmed by CT and the the small number of studies; some differences between
outcomes of the indocyanine green group were studies may influence the results. Also, the pooled data
compared with a control group. were not randomized.
CONCLUSIONS:  The result revealed that indocyanine
Funding/Support: This work was supported by grants from the Clini- green was associated with a lower anastomotic
cal Medicine Project of Jiangsu Province (BL2014023), National Natural
Science Foundation of China (No.81371683/H1819), Natural Science
leakage rate after colorectal resection. However, larger,
Foundation of Jiangsu Province (BK2016198) and National Natural Sci- multicentered, high-quality randomized controlled trials
ence Foundation of China (No. 81702592). are needed to confirm the benefit of indocyanine green
fluorescence angiography.
Financial Disclosure: None reported.

Correspondence: Tong Wang, M.D., Department of General Surgery, Wuxi

People’s Hospital Affiliated to Nanjing Medical University, Wuxi, Jiangsu KEY WORDS:  Anastomotic leakage; Colorectal cancer;
Province, 214023 People’s Republic of China. E-mail: [email protected]. Fluorescence angiography; Indocyanine green.

C
Dis Colon Rectum 2018; 61: 1228–1234
DOI: 10.1097/DCR.0000000000001123 olorectal cancer is one of the most common
Copyright © 2018 The Author(s). Published by Wolters Kluwer Health, cancers in the world, and the incidence is in-
Inc. on behalf of the American Society of Colon and Rectal Surgeons. creasing.1 With novel technical advances, better
This is an open-access article distributed under the terms of the Cre- understanding of the physiology, and improved surgical
ative Commons Attribution-Non Commercial-No Derivatives License
4.0 (CCBY-NC-ND), where it is permissible to download and share the
technical skills, surgeons offer patients better outcomes
work provided it is properly cited. The work cannot be changed in any after colorectal resections, albeit with complications.2
way or used commercially without permission from the journal. However, among postoperative complications, anasto-
1228 DISEASES OF THE COLON & RECTUM VOLUME 61: 10 (2018)
DISEASES OF THE COLON & RECTUM VOLUME 61: 10 (2018) 1229

motic leakage (AL) is the most serious complication that Search Strategy
has a negative impact on both short- and long-term out- Potential relevant studies were identified by a comprehen-
comes.3 The reported incidence rate of AL after colorec- sive literature search, which covered the following electronic
tal surgery ranges from 3% to 20%.4,5 Some studies have platforms: PubMed, Embase, Web of Science, Cochrane Li-
suggested that AL is associated with reduced overall sur- brary, and China National Knowledge Infrastructure. The
vival and increased rate of local recurrence after resec- search was performed independently by 2 researchers, and
no language or date restrictions were applied. The last search
tion for colorectal cancer.3,6
was performed in August 2017. The following terms were
Some investigators have found that poor blood supply
used during literature search: anastomotic leakage, colorectal
and tension at the anastomotic site are the main risk factors cancer, fluorescence angiography, fluorescence imaging, and
for AL.7 It has been reported that blood supply is related to indocyanine green. The reference lists of all retrieved articles
the location of the tumor, preoperative bowel obstruction, were screened to identify other relevant studies.
and perioperative transfusion.8 Moreover, absence of Rio-
lan arterial arcade and sacrifice of left colic artery during Selection Criteria
resection may also be linked with poor blood supply.9,10 Studies satisfying the following criteria were included in
A variety of methods have been used to assess the the meta-analysis: 1) comparative studies investigated
anastomotic integrity intraoperatively, including mechan- the association between ICGFA and AL in patients un-
ical patency (air leak and dye tests) and endoscopic assess- dergoing surgery for colorectal cancer, 2) the diagnosis
ment.11 Meanwhile, several clinical signs, including bowel of AL was confirmed via CT, and 3) the outcomes of the
serosal color and palpable mesenteric arterial pulsations, study cohort undergoing ICGFA were compared with a
have been used to check the vascularity of the cut end of control group in which ICGFA was not performed. Ex-
the bowel. However, these signs are subjective and may clusion criteria were publication types such as case re-
well lead to misinterpretations even by experienced sur- ports, letters reviews, meeting abstracts, meta-analyses,
geons. Moreover, some of these signs may not be feasible and proceedings, as well as studies lacking necessary data
while performing laparoscopic colon resection.1 for calculation.
Recently, many studies have found that intraoperative
indocyanine green (ICG) fluorescence angiography (ICGFA) Data Extraction and Study Quality
Data were extracted by 1 investigator with complete and in-
might be useful in preventing AL in colorectal surgery by vi-
dependent verification by another investigator. Each of the
sualizing the bowel perfusion of the anastomotic region.12,13
2 reviewers assessed the studies independently based on the
Fluorescence imaging for tissue perfusion assessment has selection criteria to collect the following descriptive infor-
repeatedly been found to be beneficial in decision-making mation from eligible studies: surname and initials of the first
and improving surgical outcomes in plastic, cardiothoracic, author, year of publication, journal, country where study
hepatobiliary, and foregut surgeries.14–18 Also in colorectal was conducted, study design, number of subjects, type of op-
surgery, ICG fluorescence imaging is useful for assessing eration, cancer type, demographic variables of the patients,
anastomotic perfusion.19 ICG is a sterile, water-soluble tri- ICG dose, and postoperative complications. Discrepancies
carbocyanine compound that absorbs near infrared light between the 2 investigators were settled by discussion. Be-
with a peak spectral absorption at 800 nm. ICG is injected cause of the mix of randomized controlled trials (RCTs) and
intravenously, which rapidly and extensively binds to plasma cohort studies, risk of bias and qualities of included studies
protein. It can be cleared by the liver in 3 to 5 minutes into were assessed using the Newcastle–Ottawa Scale.22 Studies
the bile. It is a nontoxic and nonionizing agent with a maxi- with a score of ≥7 were considered high quality.
mal daily dose of 2 mg/kg, with few reported cases of adverse
effect.20 There are few systematic reviews and meta-analyses Statistical Analysis
conducted on the effect of ICGFA in colorectal cancer sur- All of the statistical analyses were performed with Review
geries. Therefore, we aimed to analyze the current evidence Manager 5.1 (The Cochrane Collaboration, The Nordic
Cochrane Centre, Copenhagen, Denmark). The ORs and
for the impact of intraoperative ICGFA on AL after resection
95% CIs were used as the statistical measures for dichoto-
for colorectal cancer.
mous outcomes to calculate the relevance of ICGAF and
the incidence of AL after colorectal cancer. ORs were calcu-
MATERIALS AND METHODS lated from the original data and combined with the Man-
tel–Haenszel method. OR > 1.0 indicated greater risk of an
This meta-analysis was carried out in line with the Pre- adverse event in the experimental group. A p < 0.05 was
ferred Reporting Items for Systematic Reviews and Meta- considered significant for all of the analyses. Heterogeneity
Analysis statement.21 among studies was tested using χ2 and I2 statistics and the
1230 SHEN ET AL: ICGFA AND AL AFTER COLORECTAL RESECTION

Identification Records identified through Additional records identified

database searching through other sources
(n = 148) (n = 0)

Records after duplicates removed

(n = 67)
Screening

Records excluded on basis of abstract/title

(n = 23):
Records screened
(n = 14): case reports, reviews,
(n = 67)
conference abstracts
(n = 9): not related to research topics

Full-text articles assessed

for eligibility Full-text articles excluded
Eligibility

(n = 44) (n = 39):
(n = 36): not case-control study
(n = 3): lack necessary data

Studies included in
qualitative synthesis
(n = 5)
Included

Studies included in
quantitative synthesis
(meta-analysis)
(n = 4)

FIGURE 1.  Flow diagram depicting the process of selection of studies for the meta-analysis.

funnel plot. A p < 0.05 and I2 > 50% indicate significant ing studies (n = 67) were screened by title and abstract
heterogeneity. In these cases, a random-effects model was for relevance. Twenty-three studies were excluded because
used; otherwise a fixed-effect meta-analysis was performed. these were case reports, reviews, or conference abstracts
(n = 14) or not related to research topics (n = 9). Full texts
of the remaining 44 records were retrieved and evaluated.
RESULTS Among these 44 studies, 39 studies were unsuitable be-
cause of a lack of control group (n = 36) or necessary data
Description of Included Studies (n = 3). In addition, among the included 5 studies, 1 study
A total of 148 records were identified on initial searching. was excluded because the same patients were included in
After the exclusion of 81 duplicated studies, the remain- another recent study by the same authors.23,24 Finally, 4

TABLE 1.   Basic information of included studies

No. Sex NOS
Study Year Country of patients (men/women) Cancer type Operation method scorea
Kim et al24 2017 Korea 657 398/259 Rectal cancer Robot-LAR 8
Kudszus et al25 2010 Germany 402 170/232 Colorectal cancer L/C 7
Jafari et al26 2013 United States 38 28/10 Rectal cancer Robot-LAR 6
Boni et al27 2016 Italy 80 50/30 Rectal cancer L-LAR 7
LAR = low anterior resection; L = laparoscopic; C = conventional.
a
Data were calculated using the Newcastle–Ottawa Scale (NOS) for assessment of the quality of nonrandomized studies in meta-analyses.22
DISEASES OF THE COLON & RECTUM VOLUME 61: 10 (2018) 1231

ICGFA Control OR OR
Study or subgroup Events Total Events Total Weight M-H, Fixed, 95% CI Year M-H, Fixed, 95% CI
Kudszus et al25 7 201 15 201 39.0% 0.45 (0.18—1.12) 2010
Jafari et al26 1 16 4 22 8.5% 0.30 (0.03—2.98) 2013
Boni et al27 0 42 2 38 7.0% 0.17 (0.01—3.69) 2016
Kim et al24 2 310 18 347 45.5% 0.12 (0.03—0.52) 2017

Total (95% CI) 569 608 100.0% 0.27 (0.13—0.53)

Total events 10 39
Heterogeneity: χ2 = 2.48, df = 3 (p = 0.48); I2 = 0%
0.01 0.1 1 10 100
Test for overall effect: z = 3.72 (p = 0.0002)
Favors (ICGFA) Favors (control)

FIGURE 2.  Forest plot analysis. df = degrees of freedom. ICGFA = indocyanine green fluorescence angiography; MH = Mantel–Haenszel
method.

retrospective case–control studies published from 2010 to chemoradiotherapy or a complicated operation, including
2017 were incorporated into the current meta-analysis.24–27 coloanal anastomosis or inadequate perfusion.
A flow diagram of study selection is displayed in Figure 1.
The included 4 studies were from 4 different coun- ICGFA and AL After Operation of Colorectal Cancer
tries with a total sample size of 1177 patients, and all of This meta-analysis found that the use of intraoperative IC-
the studies divided samples into ICGFA group and control GFA was associated with lower incidence of AL after sur-
group. All 4 studies were retrospective case-matched and gery for colorectal cancer (Fig. 2). Among the 4 studies, the
single-institutional studies with the primary end points main outcomes were 4.0% overall reduction in leak rate
being the incidence of AL requiring surgical reinterven- and 16.4% change in surgical plan,25 12.0% overall reduc-
tion and change in the surgical strategy. Three studies tion in leak rate and 19.0% change in resection margins,26
investigated patients with rectal cancer,24,26,27 and 1 study 5.0% overall reduction in leak rate and 4.7% change in sur-
gical plan,27 and 4.9% overall reduction in leak rate.24 The
investigated patients with colorectal cancer.25 Moreover,
corresponding OR values were 0.45 (95% CI, 0.18–1.12),
the operation method differed among the studies: in 2
0.30 (95% CI, 0.03–2.98), 0.17 (95% CI, 0.01–3.69), and
studies surgeries were performed by robot-assisted laparo- 0.12 (95% CI, 0.03–0.52). The combined OR value was
scopic method,24,26 whereas in the other studies surgeries 0.27 (95% CI, 0.13–0.53). The result revealed that ICGFA
were conducted by laparoscopic/conventional method.25,27 was associated with a lower AL rate after colorectal resec-
Table 1 shows the baseline characteristics of included tion. The difference was statistically significant (p < 0.001),
studies. Two studies mentioned the use of diversion: in and there was no significant heterogeneity (χ2 = 2.48;
the study by Jafari et al,26 the rate of diversion was 75% degrees of freedom = 3; p = 0.48; I2 = 0).
in the ICG group and 77% in the control group, where
the decision to use diversion was left to the discretion of Publication Bias
the attending surgeon; in another study,24 concurrent il- From the funnel plot (Fig. 3), the included studies were of
eal diversion was performed in patients with preoperative symmetrical distribution, and the p value for the Egger test
was 0.373. Both demonstrated that there was no evidence
SE (log[OR]) of significant bias in this meta-analysis; therefore, our re-
0 sults were statistically reliable.

0.5 DISCUSSION
This meta-analysis found that use of ICGFA was associ-
1.0
ated with a lower AL rate after colorectal resection. Thus,
we conclude that intraoperative ICGFA has a link with a
lower AL rate of colorectal cancer surgery. The lower AL
1.5 rate is probably attributed to better assessment of bowel
perfusion and vascularity with the help of ICG. Moreover,
ICGFA changed the surgical plan by guiding the appropri-
2.0 ate line of bowel transection in 4.7% to 19.0% of cases.25–27
0.01 0.1 1 10 100 Recently, fluorescence angiography using ICG has
OR
become the most promising technology that allows for
FIGURE 3.  Funnel plot diagram. real-time intraoperative objective evaluation of bowel per-
1232 SHEN ET AL: ICGFA AND AL AFTER COLORECTAL RESECTION

fusion.13,26,28 A review by Mizrahi and Wexner29 pointed out

that every surgeon needs to become familiar with methods

12.0% overall reduction in

leak rate; 16.4% change

leak rate; 19.0% change

4.9% overall reduction in

4.0% overall reduction in

5.0% overall reduction in

leak rate; 4.7% change
of using ICG and its numerous clinically important ap-

in resection margins
Main outcomes

plications.29 A systematic review about near-infrared fluo-

in surgical plan

in surgical plan
rescence (NIRF) angiography in anastomotic colorectal
surgery for cancers, diverticulitis, and Crohn's disease con-
leak rate

cluded that 3.5% (31 of 894) of all NIRF patients and 7.4%
(32 of 434) of all control patients developed an anastomot-
ic leakage (p=0.002).30 Another meta-analysis including 5
in surgical

studies concluded the similar result,31 but the surgical indi-

Change

plan, %

16.4

19.0

4.7
NS

cation of one included study was not only cancer but also
IBD and diverticular disease.32 The results of non-colorec-
tal cancer surgery may affect the final statistics. In addition,
Leak rate, %

Control: 18.0

it included a study that may be outdated that we mention

Control: 5.5

6.8 min Control: 7.5

Control: 5

in the "Description of Included Studies" section.23,24 There-

ICG: 0.6

0.2-0.5 mg/kg Additional ICG: 3.5

ICG: 6.0

ICG: 0

fore, we performed the current meta-analysis to investigate

the correlation between intraoperative ICGFA and the AL
rate after colorectal resection for colorectal cancer. All 4 of
Time
NS

NS

NS

the studies showed that ICGFA reduced the AL rate after

colorectal resection. Because the difference in AL rate was
statistically significant with no significant heterogeneity or
ICG dose

bias, it is clear that ICGFA was related to a lower AL rate af-

0.2 mg/kg
6-8 mg

ter colorectal resection. We have also tried to perform some

10 mg

similar operations with the use of ICG. However, because

of several technological limitations and insufficient sample
Pulsion Medical Systems,

(Karl Storz, Tuttlingen,

angiography (IC-View,

size, our results were not as robust as the results of recent

Intuitive Surgical Inc)
Intuitive Surgical Inc,
angiography (Firefly,

angiography (Firefly,

fluorescence system
Camera system

studies. Despite this we estimated that the reduction rate

Rastatt, Germany)
Laser-assisted ICG

Laser-assisted ICG

Laser-assisted ICG

Karl Storz image1

of AL in our clinical trials was ≈4% to 6%. However, there

Sunnyvale, CA)

were differences in the included studies. Table 2 shows the

Germany)
ICG = Indocyanine green; LAR = low anterior resection; L = laparoscopic; C = conventional; NS = not stated.

detailed characteristics of these studies.

With the development of surgical techniques, many
surgeries for colorectal cancer are being increasingly per-
formed by laparoscopic and robot-assisted methods. Stud-
(average), cm
Anastomotic

Control: 5.9

Control: 7.2

ies have found good long-term results with laparoscopic

level

ICG: 5.4

ICG: 6.3

colorectal resection for colorectal cancer.33,34 On the oth-

er hand, robotic-assisted laparoscopic surgery also has
5.5
NS

shown some advantages over open surgery.35,36 However,

Surgical approach

colectomy: 63
and procedure

there was no difference between laparoscopic and robot-

and LAR: 131
Left colectomy

assisted resection in terms of postoperative AL rate.37,38

Robot-LAR

Robot-LAR
L/C right
TABLE 2.   Detailed information of included studies

Therefore, we believe that the type of operation is unlikely

L-LAR

to affect the results of this meta-analysis. Similarly, other

factors like patient demographic and preoperative charac-
teristics were considered to have no significant differences.
398/259

170/232
women)

28/10

50/30
(men/
Sex

Several limitations in this meta-analysis should be

mentioned. First, we did not take unpublished articles and
abstracts into account because the necessary data were
Control: 347

Control: 201

Control: 22

Control: 38

lacking. A second potential limitation was that, among the

ICG: 310

Kudszus et al25 ICG: 201

4 studies, the administered dose of intraoperative ICG and

ICG: 16

ICG: 42
n

camera systems were different, and whether the different

doses would influence the results needs to be confirmed.
Also, this limitation may introduce a little heterogeneity.
Jafari et al26

Boni et al27
24

Last but not least, this meta-analysis did not include RCTs,
Kim et al

and the pooled data were not randomized. Accordingly,

Study

larger, multicenter, high-quality RCTs are needed to verify

the findings of this meta-analysis.
DISEASES OF THE COLON & RECTUM VOLUME 61: 10 (2018) 1233

CONCLUSION during procedures on the rectum and colon sigmoideum. Surg

Endosc. 2017;31:S24.
This meta-analysis showed significant benefit of ICGFA in 14. Boni L, David G, Dionigi G, Rausei S, Cassinotti E, Fingerhut
reducing the incidence of AL, thereby improving patient A. Indocyanine green-enhanced fluorescence to assess bowel
outcomes. In the long term, it may offer the possibility to perfusion during laparoscopic colorectal resection. Surg Endosc.
lower the rate of mortality, as well as more promising ad- 2016;30:2736–2742.
vantages, such as lymph node evaluation. 15. Holm C, Tegeler J, Mayr M, Becker A, Pfeiffer UJ, Mühlbauer
W. Monitoring free flaps using laser-induced fluorescence of
indocyanine green: a preliminary experience. Microsurgery.
REFERENCES 2002;22:278–287.
16. Hutteman M, van der Vorst JR, Mieog JS, et al. Near-infrared
1. James DR, Ris F, Yeung TM, et al. Fluorescence angiography
fluorescence imaging in patients undergoing pancreaticoduo-
in laparoscopic low rectal and anorectal anastomoses with
pinpoint perfusion imaging: a critical appraisal with specific denectomy. Eur Surg Res. 2011;47:90–97.
focus on leak risk reduction. Colorectal Dis. 2015;17(suppl 17. Shimada Y, Okumura T, Nagata T, et al. Usefulness of blood sup-
3):16–21. ply visualization by indocyanine green fluorescence for recon-
2. Montedori A, Cirocchi R, Farinella E, Sciannameo F, Abraha I. struction during esophagectomy. Esophagus. 2011;8:259–266.
Covering ileo- or colostomy in anterior resection for rectal car- 18. Waseda K, Ako J, Hasegawa T, et al. Intraoperative fluorescence
cinoma. Cochrane Database Syst Rev. 2010;(5):CD006878. imaging system for on-site assessment of off-pump coronary
3. Goto S, Hasegawa S, Hida K, et al.; Study Group for Nomogram artery bypass graft. JACC Cardiovasc Imaging. 2009;2:604–612.
of the Japanese Society for Cancer of the Colon and Rectum. 19. Wada T, Kawada K, Takahashi R, et al. ICG fluorescence imag-
Multicenter analysis of impact of anastomotic leakage on long- ing for quantitative evaluation of colonic perfusion in laparo-
term oncologic outcomes after curative resection of colon can- scopic colorectal surgery. Surg Endosc. 2017;31:4184–4193.
cer. Surgery. 2017;162:317–324. 20. Alander JT, Kaartinen I, Laakso A, et al. A review of indocya-
4. Kang CY, Halabi WJ, Chaudhry OO, et al. Risk factors for anas- nine green fluorescent imaging in surgery. Int J Biomed Imaging.
tomotic leakage after anterior resection for rectal cancer. JAMA 2012;2012:940585.
Surg. 2013;148:65–71. 21. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Pre-
5. Park JS, Choi GS, Kim SH, et al. Multicenter analysis of risk fac- ferred reporting items for systematic reviews and meta-analyses:
tors for anastomotic leakage after laparoscopic rectal cancer ex- the PRISMA statement. J Clin Epidemiol. 2009;62:1006–1012.
cision: the Korean laparoscopic colorectal surgery study group. 22. Stang A. Critical evaluation of the Newcastle-Ottawa scale for
Ann Surg. 2013;257:665–671. the assessment of the quality of nonrandomized studies in me-
6. Sammour T, Hayes IP, Jones IT, Steel MC, Faragher I, Gibbs P. ta-analyses. Eur J Epidemiol. 2010;25:603–605.
Impact of anastomotic leak on recurrence and survival after 23. Kim JC, Lee JL, Yoon YS, Alotaibi AM, Kim J. Utility of indocy-
colorectal cancer surgery: a BioGrid Australia analysis. ANZ J anine-green fluorescent imaging during robot-assisted sphinc-
Surg. 2018;88:E6–E10. ter-saving surgery on rectal cancer patients. Int J Med Robot.
7. Trencheva K, Morrissey KP, Wells M, et al. Identifying important 2016;12:710–717.
predictors for anastomotic leak after colon and rectal resection: 24. Kim JC, Lee JL, Park SH. Interpretative guidelines and possi-
prospective study on 616 patients. Ann Surg. 2013;257:108–113. ble indications for indocyanine green fluorescence imaging in
8. García-Granero E, Navarro F, Cerdán Santacruz C, et al. Indi- robot-assisted sphincter-saving operations. Dis Colon Rectum.
vidual surgeon is an independent risk factor for leak after dou- 2017;60:376–384.
ble-stapled colorectal anastomosis: an institutional analysis of 25. Kudszus S, Roesel C, Schachtrupp A, Höer JJ. Intraoperative
800 patients. Surgery. 2017;162:1006–1016. laser fluorescence angiography in colorectal surgery: a nonin-
9. Huang J, Zhou J, Wan Y, et al. Influences of inferior mesenteric vasive analysis to reduce the rate of anastomotic leakage. Lan-
artery types and Riolan artery arcade absence on the incidence genbecks Arch Surg. 2010;395:1025–1030.
of anastomotic leakage after laparoscopic resection of rec- 26. Jafari MD, Lee KH, Halabi WJ, et al. The use of indocyanine
tal cancer [in Chinese]. Zhonghua Wei Chang Wai Ke Za Zhi. green fluorescence to assess anastomotic perfusion dur-
2016;19:1113–1118. ing robotic assisted laparoscopic rectal surgery. Surg Endosc.
10. Zang L, Ma J, Zheng M. Effect of preserving left colic artery dur- 2013;27:3003–3008.
ing radical operation of rectal cancer on anastomotic leakage 27. Boni L, Fingerhut A, Marzorati A, Rausei S, Dionigi G, Cassino-
and operation time [in Chinese]. Zhonghua Wei Chang Wai Ke tti E. Indocyanine green fluorescence angiography during lapa-
Za Zhi. 2016;19:386–387. roscopic low anterior resection: results of a case-matched study.
11. Nachiappan S, Askari A, Currie A, Kennedy RH, Faiz O. Intra- Surg Endosc. 2017;31:1836–1840.
operative assessment of colorectal anastomotic integrity: a sys- 28. Sujatha-Bhaskar S, Jafari MD, Stamos MJ. The role of fluo-
tematic review. Surg Endosc. 2014;28:2513–2530. rescent angiography in anastomotic leaks. Surg Technol Int.
12. Marquardt C, Krauth C, Koppes P, Kristen R, Schiedeck T. In- 2017;30:83–88.
traoperative fluorescence angiography with indocyanine green: 29. Mizrahi I, Wexner SD. Clinical role of fluorescence imaging in
influence on anastomotic leak rate in colorectal resections. Co- colorectal surgery: a review. Expert Rev Med Devices. 2017;14:75–82.
loproctology. 2017;39:265–270. 30. van den Bos J, Al-Taher M, Scholas RM, van Kuijk S, Bouvy ND,
13. Bencurik V, Škrovina M, Bartoš J, et al. Evaluation of intestinal Stassen LPS. Near-infrared fluorescence imaging for real-time
perfusion by Indocyanine Green (ICG) fluorescence imaging intraoperative guidance in anatomotic colorectal surgery: a
1234 SHEN ET AL: ICGFA AND AL AFTER COLORECTAL RESECTION

systematic review of literature. J Laparoendosc Adv Surg Tech. a retrospective analysis of 121 sphincter-saving procedures in a
2018;28:157–167. single institution. Surg Endosc. 2011;25:454–462.
31. Blanco-Colino R, Espin-Basany E. Intraoperative use of ICG 35. Zimmern A, Prasad L, Desouza A, Marecik S, Park J, Abcarian
fluorescence imaging to reduce the risk of anastomotic leakage H. Robotic colon and rectal surgery: a series of 131 cases. World
in colorectal surgery: a systematic review and meta-analysis. J Surg. 2010;34:1954–1958.
Tech Coloproctcol. 2018;22:15–23. 36. Ragupathi M, Ramos-Valadez DI, Miller S, Haas EM. The safety
32. Kin C Vo H, Welton L, Welton M. Equivocal effect of intraoper- and efficacy of robotic-assisted laparoscopic surgery for com-
ative fluorescence angiography on colorectal anastomotic leaks. plex colorectal procedures. Surg Endosc. 2011;25:S280.
Dis Colon Rectum. 2015;58:582–587. 37. Bello B, Umanskiy K, Ohara K, et al. Robotic versus laparoscopic
33. MacDonald E, Molloy R. Laparoscopic versus open resection proctectomy for rectal cancer: short-term outcomes and cost
for colorectal cancer: early outcome data from a large regional analysis of a case matched series. Dis Colon Rectum. 2013;56:e115.
database. Surg Endosc. 2012;26:S182–S183. 38. Halabi WJ, Kang CY, Jafari MD, et al. Robotic-assisted colorec-
34. Lam HD, Stefano M, Tran-Ba T, Tinton N, Cambier E, Navez B. tal surgery in the United States: a nationwide analysis of trends
Laparoscopic versus open techniques in rectal cancer surgery: and outcomes. World J Surg. 2013;37:2782–2790.

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required! Access DC&R journal content on the go, plus these features:
ࡄ Podcasts
ࡄ Clinical Practice Guidelines Collection
ࡄ Visual Abstract Infographics
ࡄ Tips for Submitting to DC&R
ࡄ Video Introduction to each Issue from the Editor-in-Chief
ࡄ Video Abstracts and Video Vignettes
ࡄ Entire Archive of DC&R content back to 1958
ࡄ Links to Residents Corner and CME
ࡄ Legislative updates
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Visit dcrjournal.com today.
Access is a subscriber and ASCRS member benefit.

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