International Journal of Colorectal Disease (2023) 38:52

https://doi.org/10.1007/s00384-023-04328-6

REVIEW

Surgical approaches to colonic and rectal anastomosis: systematic

review and meta‑analysis
Ana Oliveira1,2,3   · Susana Faria4   · Nuno Gonçalves1,2   · Albino Martins2,3   · Pedro Leão1,2 

Accepted: 28 January 2023

© The Author(s) 2023

Abstract
Purpose  Postoperative complications after a colonic and rectal surgery are of significant concern to the surgical community.
Although there are different techniques to perform anastomosis (i.e., handsewn, stapled, or compression), there is still no
consensus on which technique provides the least number of postoperative problems. The objective of this study is to compare
the different anastomotic techniques regarding the occurrence or duration of postoperative outcomes such as anastomotic
dehiscence, mortality, reoperation, bleeding and stricture (as primary outcomes), and wound infection, intra-abdominal
abscess, duration of surgery, and hospital stay (as secondary outcomes).
Methods  Clinical trials published between January 1, 2010, and December 31, 2021, reporting anastomotic complications
with any of the anastomotic technique were identified using the MEDLINE database. Only articles that clearly defined the
anastomotic technique used, and report at least two of the outcomes defined were included.
Results  This meta-analysis included 16 studies whose differences were related to the need of reoperation (p < 0.01) and the
duration of surgery (p = 0.02), while for the anastomotic dehiscence, mortality, bleeding, stricture, wound infection, intra-
abdominal abscess, and hospital stay, no significant differences were found. Compression anastomosis reported the lowest
reoperation rate (3.64%) and the handsewn anastomosis the highest (9.49%). Despite this, more time to perform the surgery
was required in compression anastomosis (183.47 min), with the handsewn being the fastest technique (139.92 min).
Conclusions  The evidence found was not sufficient to demonstrate which technique is most suitable to perform colonic
and rectal anastomosis, since the postoperative complications were similar between the handsewn, stapled, or compression
techniques.

Keywords  Anastomosis · Colon · Rectum · Handsewn · Stapled · Compression

Introduction

Anastomotic dehiscence after colonic and rectal resection

* Pedro Leão
pedroleao@med.uminho.pt
1
Life and Health Sciences Research Institute (ICVS), School
of Medicine, University of Minho, Braga 4710‑057, Portugal
2
ICVS/3B’s-PT Government Associate Laboratory,
Braga/Guimarães, Portugal
3
3B’s Research Group, I3Bs – Research Institute
on Biomaterials, Biodegradables & Biomimetics;
Headquarters of the European Institute of Excellence
on Tissue Engineering & Regenerative Medicine, University
of Minho, AvePark‑Parque de Ciência e Tecnologia, Zona
Industrial da Gandra, Barco, Guimarães 4805‑017, Portugal
4
Centre of Mathematics (CMAT), Department
of Mathematics, University of Minho, Guimarães 4800‑058,
Portugal
is a dreaded complication with increased morbidity and sig-
nificant mortality rate, ranging from 6 to 22% depending
on the anastomotic site [1]. The consequences of an inef-
fective surgery can be so diverse and devastating that, in
addition to the fearsome anastomotic leakage, this situation
can also cause the appearance of bleeding, strictures, and
intra-abdominal and wound infections [2–5]. Late diagnosis
can even lead to cases of generalized peritonitis progressing
to sepsis, compromising the patient’s life. It may require
reoperation and, consequently, an increase in hospital stay
with inevitable extra economic costs [2, 6].
Several aspects have been identified as possible pre-
dictors of anastomotic complications, being divided in
patient-related risk factors [7–10] and surgical procedure’s

13
Vol.:(0123456789)
 52   Page 2 of 24
characteristics [11, 12]. Focusing on the surgery itself, dif-
ferent techniques can be used to perform colonic and rectal
anastomosis, namely handsewn, stapled, or compression.
The handsewn and stapled techniques are the most com-
monly used, although associated with the idea that the
introduction of foreign materials can injure the intestinal
tissue and trigger an inflammatory response [2, 13, 14].
Despite handsewn anastomosis be a traditional technique,
the stapled anastomosis has become very attractive due to
its ease implementation. By its side, compression anasto-
mosis involves the use of devices, such as clips and rings,
to perform an end-to-end sutureless anastomosis. The
intestinal segments are compressed by these devices that
place the ends in apposition. Afterwards, the devices are
expelled spontaneously by the body. Although compres-
sion anastomosis is considered safe, it has not yet achieved
considerable popularity among the surgical community
[15–19]. Despite all those scientific evidences, there is no
consensus concerning the most advantageous technique to
perform a colonic and rectal anastomosis. Despite differ-
ent technical characteristics and handling skills, there is no
specific guidance regarding the technique that should be
used, and these decisions have been based on the surgeon’s
experience and preference [5, 14, 18, 20]. Therefore, stud-
ies comparing the three anastomotic techniques indepen-
dently are needed to guide the medical community towards
the most suitable technique. In addition, these analyses
should not be restricted to studies that compare more than
one technique, otherwise a large part of the sample will
not be included.
In this systematic review and meta-analysis, we intended
to understand which technique is the most successful to
perform a colonic and rectal anastomosis, providing fewer
postoperative complications.
Methods
Search strategy
A literature search was conducted using the MEDLINE data-
base for studies published between January 1, 2010, and
December 31, 2021, using the following combinations of
keywords:
1. colon AND anastomosis AND dehiscence
2. colon AND anastomosis AND suture
3. colon AND anastomosis AND infection
4. colon AND anastomosis AND inflammation
The search was restricted to English language publica-
tions describing clinical investigations in humans, more
13
International Journal of Colorectal Disease (2023) 38:52
specifically, clinical trials. The studies included comply with
the Preferred Reporting Items for Systematic Reviews and
Meta-analysis (PRISMA) methodology [21].
Data collection and analysis
Three authors selected the studies independently. The data
were extracted and verified independently by each one. The
final data were combined and analyzed.
Types of outcome measures
Anastomotic dehiscence, mortality, reoperation, bleed-
ing, and stricture represented the primary outcomes, while
wound infection, intra-abdominal abscess, duration of sur-
gery, and hospital stay were defined as secondary outcomes.
Primary outcomes
• Anastomotic dehiscence: dehiscences or leaks diagnosed
clinically through the discharge of feces at the anastomo-
sis site, identified radiologically, through the presence of
leakage with the postoperative control enema in a patient
who had no evidence of a clinical anastomotic leakage,
or by operative confirmation.
• Mortality: postoperative deaths due to anastomotic com-
plications.
• Reoperation: surgical reintervention due to an anasto-
motic complication that cannot be treated conservatively.
• Bleeding: postoperative bleeding or hemorrhage that
occurs from the anastomotic site or in the abdominal
cavity.
• Stricture: narrowing in the intestinal lumen as a result of
anastomotic healing.
Secondary outcomes
• Wound infection: the presence of infection in the abdomi-
nal wound.
• Intra-abdominal abscess: the accumulation of fluids in
the abdominal cavity.
• Duration of surgery: time to perform the entire surgical
procedure, including anastomosis.
• Hospital stay: time from surgery to hospital discharge.
Inclusion criteria
Only articles that clearly defined the type of anastomosis
used (handsewn, stapled, or compression), and report at least
two of the outcomes defined above.
International Journal of Colorectal Disease (2023) 38:52 Page 3 of 24  52
Exclusion criteria
Exclusion criteria were (1) procedures without anastomosis
of the colon or rectum; (2) emergency surgery or no clari-
fication on its origin; (3) investigation of new diagnostic
methods; (4) approaches that deviate from clinical practice
in the handsewn and stapled techniques, by implementing
new methods, therapies or devices; and (5) no results for at
least two study outcomes.
Data extraction
Some data was extracted from the studies, such as first
author and year of publication, trial registration, study
design, time of perspective, randomization, number of
patients included, objective, study groups, age and sex of the
patients, type of anastomosis, anastomotic site, procedure,
Fig. 1  PRISMA flowchart: selection of relevant studies
surgical approach, characteristics of anastomosis, diagnos-
tic methods, other relevant procedures, bowel preparation
and prophylaxis, endpoints of the study, and main results.
The total number of patients who respond to the outcomes
defined above were also extracted, as well as the duration of
surgery and length of hospital stay.
Statistical analysis
The meta-analysis was conducted using the “meta” package
(version 4.18.0, 2021) in R (The R Foundation for Statistical
Computing; version 4.0.4, 2021).
For the duration of surgery and hospital stay outcomes,
results are presented as means with an associated 95% con-
fidence interval (CI). Study data presented as median and
ranges were converted to mean and standard deviation (SD)
using the method developed by Wan et al. [22]. For the other
13
 Table 1  Characteristics and patient demographic data of the included studies
52  

Source Trial registration Study design Time of Randomization Number Objective Groups Age (years), Sex, n Type of
perspective of cases mean ± SD anastomosis
Male Female

13
Ferrer-Márquez NTC03990714 Multicenter Prospective Yes 160 Evaluation of short- IA (n = 82); EA IA: 70.51 ± 9.88; IA: 43; EA: 39 IA: 39; EA: 39 Stapled
et al. (2021) term outcomes (n = 78) EA:
Page 4 of 24

[26] of performing 68.65 ± 12.51

intracorporeal
anastomosis
(IA) versus
extracorporeal
anastomosis (EA) in
laparoscopic right
hemicolectomy for
right colon neoplasm
Milone et al. NCT03422588 Single institution Prospective Yes 59 Evaluation of the IA (n = 30); EA IA: 65.26 (4.42); IA: 13; EA: 13 IA: 17; EA: 16 Stapled
(2021) [27] surgical stress (n = 29) EA: 66.30 (4.19)
response and the
metabolic response
in patients who
underwent right
colonic resection for
colon cancer
Mai-Phan et al. - Non-blind, single Prospective Yes 122 Evaluation of the MBP (n = 62); MBP: 57.0 ± 14.8; MBP: 27; MBP: 35; Handsewn
(2019) [28] center effect of mechanical No-MBP No-MBP: No-MBP: 33 No-MBP: 27
bowel preparation (n = 60) 58.2 ± 14.3
(MBP) on elective
laparoscopic
colectomy
Jurowich et al. - - Retrospective No 4062 Assessment whether Handsewn Handsewn: Handsewn: 1293; Handsewn: 1449; Handsewn and
(2019) [29] the anastomotic (n = 2742); 72.9 ± 10.9; Stapled: 622 Stapled: 698 stapled
technique (handsewn Stapled Stapled:
or stapled) (n = 1320) 73.9 ± 10.6
after open right
hemicolectomy for
right-sided colonic
cancer influences
postoperative
complications
Bakker et al. NTR3080 Non-blind, Prospective Yes 402 Evaluation of the C-seal (n = 202); C-seal: 66; C-seal: 121; C-seal: 81; Stapled
(2017) [30] multicenter efficacy of the No C-seal, Control: 64 Control: 120 Control: 80
C-seal in reducing Control
anastomotic leakage (n = 200)
International Journal of Colorectal Disease

in stapled colorectal
anastomosis
(2023) 38:52
 Table 1  (continued)
Source Trial registration Study design Time of Randomization Number Objective Groups Age (years), Sex, n Type of
perspective of cases mean ± SD anastomosis
Male Female

Herrle et al. NCT00996554 Double-blind, Prospective Yes 252 Evaluation of the SLA (n = 129); SLA: 67.7 ± 11.1; SLA: 72; DLA: SLA: 57; DLA: Handsewn
(2016) [3] multicenter complication rates DLA (n = 123) DLA: 64.6 ± 13.4 69 54
after hand-sutured
continuous single-
layer anastomosis
(SLA) with
continuous double-
layer colo-colonic
and ileocolonic
anastomosis (DLA)
International Journal of Colorectal Disease

in elective colorectal
surgery
Frasson et al. - Observational, Prospective No 1102 Determination of Handsewn 74 (66–80) 622 480 Handsewn and
(2016) [31] multicenter pre-/intraoperative (n = 324); stapled
risk factors for Stapled
anastomotic leakage (n = 778)
after elective right
(2023) 38:52

colon resection for

cancer
Matsuda et al. MIN00000848 Single-blind, Prospective Yes 40 Evaluation of short- Isoperistaltic Antiperistaltic Antiperistaltic Antiperistaltic Stapled
(2015) [32] single center term outcomes SSSA (n = 20); SSSA: 68 ± 10; SSSA: 11; SSSA: 9;
of isoperistaltic Antiperistaltic Isoperistaltic Isoperistaltic Isoperistaltic
stapled side-to-side SSSA (n = 20) SSSA: 66 ± 12 SSSA: 11 SSSA: 9
anastomosis (SSSA)
comparing them
with antiperistaltic
SSSA during colon
cancer surgery
D’Hoore et al. NCT01091155 Non-blind, Prospective No 266 Evaluation of - 62 138 128 Compression
(2015) [4] multicenter ColonRing™
performance in
(low) colorectal
anastomosis
Placer et al. - Single-blind, Prospective Yes 281 Evaluation of the BSLR (n = 136); BSLR: 67; Control: BSLR: 88; BSLR: 48; Stapled
(2014) [33] single center effectiveness of Control 66 Control: 90 Control: 55
bioabsorbable staple (n = 145)
line reinforcement
(BSLR) in
reducing colorectal
anastomotic
complications
Page 5 of 24 
52

13
 Table 1  (continued)
52  

Source Trial registration Study design Time of Randomization Number Objective Groups Age (years), Sex, n Type of
perspective of cases mean ± SD anastomosis
Male Female

13
Leung et al. - Double-blind Prospective Yes 70 Comparison of the HNC (n = 35); HNC: 62; CL: 72 HNC: 13; CL: 12 HNC: 22; CL: 23 Stapled
(2013) [34] short-term outcomes CL (n = 35)
Page 6 of 24

of patients who
underwent hybrid
NOTES colectomy
(HNC) with those
who underwent
conventional
laparoscopic
colectomy (CL)
Khromov et al. - Non-blind, Prospective No 40 Evaluation of the - 65.8 18 22 Compression
(2013) [35] multicenter short-term clinical
outcome and safety
profile of the
NiTi Biodynamix
ColonRing™
compression
anastomosis in
elective colorectal
resection
Ruiz-Tovar et al. NCT01458353 Blinded for Prospective Yes 84 Prospective evaluation Stapled (n = 42); Stapled: Stapled: 26; Stapled: 16; Handsewn and
2012 [36] results analysis, of the peritoneal Handsewn 68.5 ± 10.2; Handsewn: 25 Handsewn: 17 stapled
single center contamination after (n = 42) Handsewn:
the performance of 69.9 ± 11.5
stapled or handsewn
anastomosis and if
these data correlate
with a surgical-site
infection
Zurbuchen et al. ISRCTN-45665492 Single-blind, Prospective Yes 67 Investigation whether Side-to-side Side-to-side: Side-to-side: 17; Side-to-side: 19; Handsewn and
(2013) [37] multicenter stapled side-to- (n = 36); end- 39.5 ± 12.55; end-to-end: 19 end-to-end: 12 stapled
side anastomosis, to-end (n = 31) end-to-end:
compared to the 39.1 ± 12.58
handsewn end-to-
end anastomosis,
results in a
decreased recurrence
of Crohn’s disease
following ileocolic
resection
International Journal of Colorectal Disease

Bertani et al. - Single center Prospective Yes 229 Evaluation of Preoperative MBP: 63; no-MBP: MBP: 65; MBP: 49; Stapled
(2011) [38] the impact of MBP plus a 64 no-MBP: 60 no-MBP: 55
preoperative MBP glycerine 5%
for colon and rectal enema, MBP
cancer surgery in (n = 114);
comparison with Single
(2023) 38:52

a single glycerine glycerine

enema 5% enema,
no-MBP
(n = 115)
 International Journal of Colorectal Disease (2023) 38:52 Page 7 of 24  52

outcomes, the results are presented as proportions with asso-

Compression
anastomosis
Type of
ciated 95% CI. The Mantel–Haenszel statistical method was
applied for dichotomous outcomes. Continuous outcomes
were analyzed using the mean difference (MD) with an asso-
ciated 95% CI and pooled using an inverse variance model.
The subgroup analysis was performed based on the type
of anastomotic technique (handsewn, stapled, or compres-
Female

sion). Studies in which the outcome of interest was not

14

observed in either group were excluded from the meta-

analysis of that income. p < 0.05 was considered to indicate
statistical significance.
Sensitivity analysis was performed by excluding one
Sex, n

Male

study from the data set to investigate its influence on the

9

overall results, and explore sources of significant heteroge-

neity. Considering the heterogeneity of the clinical studies,
Age (years),
mean ± SD

which refers to diversity relevant to complicated clinical

situations, we used the random-effects model based on the
60

Sidik-Jonkman method [23]. An inverse-variance random-

effects model was used for all analyses. Heterogeneity
between studies was assessed using the I2 statistics (hetero-
geneities < 25%, 25–50%, and > 50% were considered as low,
Groups

moderate, and high, respectively [24]) and Chi-square test

-

( 𝜒 2 ), with p < 0.05 considered statistically significant.

Tests for funnel plot asymmetry were used in each out-
undergoing a left-
device in patients

sided colectomy
outcomes of the

27 compression
Evaluation of the

come when there were at least ten studies included in the

NiTi CAR™

anastomosis

meta-analysis [25]. Egger’s test was used to assess potential

Objective

publication bias via funnel plost asymmetry.

Number
of cases

Results
23

The literature search identified a total of 74 studies. Of these

Randomization

studies, 14 corresponded to the first combination of key-

words, 14 to the second, 40 to the third, and 6 to the fourth.
Additionally, six articles were included through the analy-
No

sis of reference lists. However, ten duplicate studies were

removed, leaving a total of 70 studies for screening accord-
perspective

Pilot study, single Prospective

ing to Fig. 1. In this analysis, 16 studies were included, com-

Time of

prising a total of 7259 patients. Of these, two studies had

a handsewn anastomosis, seven stapled, three by compres-
sion, and four included both handsewn and stapled. Over-
Study design

all, 3513 patients underwent handsewn anastomosis, 3417

center

stapled, and 329 compression. The reinforcement groups

of the studies included in the stapled technique were not
included, and the analysis was restricted to 3079 patients.
Trial registration

The characteristics of studies and patient demographics are

shown in Table 1.
Studies reporting emergency surgeries were not con-
Table 1  (continued)

sidered due to the higher rates of anastomotic complica-

-

tions and because they did not provide relevant informa-

Buchberg et al.
(2011) [18]

tion regarding mechanical bowel preparation and additional

prophylaxis. Studies investigating new diagnostic techniques
Source

were not included due to the impossibility of knowing which

13
 Table 2  Main characteristics and results of included studies
52  

Source Site Procedure Surgical approach Characteristics of Diagnostic Other procedures Bowel Study endpoints Main results
anastomosis methods preparation and

13
prophylaxis

Ferrer-Márquez Colon Right Laparoscopy Stapled (side-to- - - No bowel Paralytic ileus, Median of hospital
Page 8 of 24

et al. (2021) [26] hemicolectomy side) preparation; surgical-site stay: 7 days (both
for right colon intravenous infection, hospital groups). Paralytic
neoplasm antibiotics stay, anastomotic ileus: 20.63%.
preoperatively leakage, repeat Surgical-site
interventions, infection: 10%
postoperative (3.65% IA, 16.67%
pain EA). Anastomotic
leakage: 6.25%
Milone etal. (2021)  Colon Elective Laparoscopy Stapled - - Not mentioned Levels of IL-6, Proinfammatory
[27] (extracorporeal C-reactive mediator IL-6,
side-to-side protein (CRP), CRP, TNF and
isoperistaltic IL-1β, IL-10, IL-1β levels were
anastomosis IL-13, tumor significantly
or side-to-side necrosis factor α reduced in IA
isoperistaltic (TNFα), cortisol compared to EA.
anastomosis) and insulin An improved
profile of the
anti-inflammatory
cytokines IL-10
and IL-13 was
observed in the
IA group. Cortisol
was increased in
EA, while insulin
was reduced in the
EA group
Mai-Phan et al. Colon Elective colon Laparoscopy Handsewn (1 and 2 CT scan, - MBP (sodium Anastomotic Abdominal
(2019) [28] surgery layers) laparotomy, phosphate or leakage, surgical- complications
ultrasonography, polyethylene site infection, (anastomotic leak
clinical glycol); extra-abdominal and surgical-site
examination, lab intravenous complications, infection): 16.2%
tests, imaging antibiotic hospital stay, MBP, 18.3%
tests prophylaxis death no-MBP.
International Journal of Colorectal Disease

Anastomotic
leakage: 6.5%
MBP, 3.3% no-
MBP. Hospital
stay: 9.0 ± 2.9
(2023) 38:52

MBP, 8.4 ± 1.9
no-MBP
 Table 2  (continued)
Source Site Procedure Surgical approach Characteristics of Diagnostic Other procedures Bowel Study endpoints Main results
anastomosis methods preparation and
prophylaxis

Jurowich et al. Colon Elective and open Laparotomy Handsewn; Stapled - - Not mentioned Anastomotic Anastomotic
(2019) [29] right (any type of leakage, leakage: 3.9%
hemicolectomy stapler device) postoperative handsewn, 3.0%
for right-sided ileus, stapled.
colonic cancer reoperation, Postoperative
surgical-site ileus: 4.0%
infection, handsewn, 3.6%
hospital stay, stapled.
International Journal of Colorectal Disease

death Reoperation: 9.6%

handsewn, 10.5%
stapled.
Superficial site
infection: 10.2%
handsewn, 9.5%
(2023) 38:52

stapled.
Postoperative
bleeding: 1.8%
handsewn, 1.6%
stapled.
Duration of
surgery:
134.1 ± 49.0
handsewn,
120.5 ± 46.5
stapled. Hospital
stay: 13.4 ± 9.2
handsewn,
13.6 ± 9.5
handsewn.
Mortality: 2.9%
handsewn, 3.6%
stapled
Bakker et al. Colorectal Elective surgery Laparotomy; Stapled (circular; Air leak test - Mechanical oral Anastomotic Overall anastomotic
(2017) [30] with a stapled laparoscopy; C-seal: bowel leakage leakage: 7.7%.
colorectal conversion biodegradable preparation Anastomotic
anastomosis polyurethane; leakage: 10.4%
end-to-end, end- C-seal, 5.0%
to-side, side-to- control
end, side-to-side)
Page 9 of 24 
52

13
 Table 2  (continued)
52  

Source Site Procedure Surgical approach Characteristics of Diagnostic Other procedures Bowel Study endpoints Main results
anastomosis methods preparation and

13
prophylaxis

Herrle et al. (2016) Colorectal Elective colorectal Laparotomy; Handsewn (2 Endoscopy, CT - Not mentioned Clinical Clinical anastomotic
[3] surgery laparoscopy; layers; scan, reoperation anastomotic leakage: 3.1%
Page 10 of 24

conversion continuous; leakage, duration SLA, 4.9% DLA

4–0, 5–0 of anastomotic (not significant
polydioxanone, suture, morbidity, - NS). Suture
ETHICON; 1 stool patterns duration: 18 min
layer, 4–0 PDS, SLA, 24 min
ETHICON; DLA. Subjective
end-to-end, end- well-being and
to-side) stool patterns: NS
Frasson et al. Colon Elective right colon Laparotomy; End-to-end, end- - Suture Not mentioned Preoperative risk Anastomotic
(2016) [31] resection for laparoscopy; to-side, side-to- reinforcement factors for leakage: 8.4%.
cancer conversion end, side-to-side with allogenic anastomotic Radiological/
or synthetic leakage, wound surgical
material was infection, intervention: 6.5%.
performed on morbidity, Morbidity: 29.0%.
0.3% of patients mortality Mortality: 2.6%.
Wound infection:
13.4%
Matsuda et al. Colon Elective curative Laparotomy; Stapled (linear, - Additional hand MBP Anastomotic Anastomotic
(2015) [32] resection after laparoscopy Echelon sutures for (polyethylene leakage, leakage: 2
colon cancer Endopath; reinforcement (1 glycol); hemorrhage, isoperistaltic
side-to-side) layer, 4–0 PDS intravenous stenosis, wound SSSA, 0
II, ETHICON) antibiotic infection, antiperistaltic SSSA
prophylaxis prolonged ileus, (NS, p = 0.487).
(flomoxef intra-abdominal Anastomotic
sodium) abscess, first stenosis: 1
defecation after antiperistaltic
surgery, SSSA, 0
reoperation, isoperistaltic SSSA.
hospital stay No anastomotic
hemorrhage in
either group.
Hospital stay: NS
International Journal of Colorectal Disease

D’Hoore et al. Colorectal Open or Laparotomy; Compression Air leak test, Additional MBP; antibiotic Anastomotic Overall anastomotic
(2015) [4] laparoscopic laparoscopy; (ColonRing™; contrast reinforcement or prophylaxis; leakage leakage: 5.3%
left‐sided conversion end‐to‐end, insufflation reconstruction thrombosis (3.1% for low
colorectal colonic pouch test, endoscopy and/or fecal prophylaxis anastomosis).
resection with reconstruction) (rigid or flexible deviation when Septic anastomotic
(2023) 38:52

the creation of an sigmoidoscopy), leak test was complications:

anastomosis radiography positive 8.3% (8.2% of low
anastomosis)
 Table 2  (continued)
Source Site Procedure Surgical approach Characteristics of Diagnostic Other procedures Bowel Study endpoints Main results
anastomosis methods preparation and
prophylaxis

Placer et al. (2014) Colorectal Left colon resec- Laparotomy; lapa- Stapled (circular, Air leak test, - MBP; antibiotic Pooled incidences Pooled incidences
[33] tion for a benign roscopy proximate, BSLR imaging tests, prophylaxis; of anastomotic of anastomotic
or malignant device-Gore visual control, antithromboem- complications complications (NS,
condition and Seamguard: syn- colon and tissue bolic prophy- (leakage, bleed- p = 0.821). Leak-
elective colorec- thetic bioabsorb- doughnut integ- laxis; anti- ing, or stenosis), age: 6.6% vs 4.8%
tal anastomosis able polyglycolic rity, proctosig- inflammatory reoperations, (NS, p = 0.518).
acid/trimethyl- moidoscopy prophylaxis hospital stay Hemorrhage:
ene carbonate (dexamethasone, 1.4% vs 1.3%
International Journal of Colorectal Disease

copolymer fiber; carbohydrate- (NS, p = 0.431).

2 layers; side-to- rich drink) Stenosis: 2.9%
end) vs 6.8% (NS,
p = 0.128) Hospital
stay: 7 days (NS,
p = 0.242). Reoper-
(2023) 38:52

ation:7.3% vs 9.6%
(NS, p = 0.490).
Mortality: 0.3%
control
Leung et al. (2013) Colorectal Left-sided colonic Laparoscopy Stapled (circular; Air leak test, - MBP; antibiotic Operating time, Operating time:
[34] tumor without mini- side-to-end, end- colonoscopy, prophylaxis blood loss, 105 vs. 100 min
laparotomy; to-end) histopathologic length of hospital (p = 0.851).
laparoscopy with examination stay, pain score, Blood loss: 30 vs.
mini-laparotomy wound infection 30 ml (p = 0.954).
Hospital stay: 5 vs.
5 days (p = 0.990).
Maximum pain
score during the
first week: 1 vs.
2 (p = 0.017).
No patients in
the HNC group
developed wound
infection, whereas
four patients in the
CL group did so
(p = 0.005)
Page 11 of 24 
52

13
 Table 2  (continued)
52  

Source Site Procedure Surgical approach Characteristics of Diagnostic Other procedures Bowel Study endpoints Main results
anastomosis methods preparation and

13
prophylaxis

Khromov et al. Colorectal Elective colorectal Laparotomy; Compression Air leak test, Additional Enemas; MBP Anastomotic Duration of
(2013) [35] resection with laparoscopy (Biodynamix betadine reinforcing (oral leakage, hospital surgery: 120 min.
Page 12 of 24

the Biodynamix ColonRing™) (povidone- sutures polyethylene stay, time to first Anastomotic time:
­ColonRingTM iodine) glycol); passage of flatus 14.8 min. Height
compression instillation, intravenous and stool and to of anastomosis
anastomosis ring macroscopic antibiotic oral intake, from the anal
and histological prophylaxis anastomotic verge: 18.2 cm.
assessment of (cephalosporins, stenosis, wound Time to the
the integrity of garamicin) infection, passage of first
the doughnuts, reoperation flatus and first
proctoscopic stool: 2.4 and
examination, CT 3.5 days,
scan respectively.
Hospital stay:
7.3 days.
Anastomotic
leakage: 5%.
Wound infection:
5%. No
anastomotic
stricture. There
was one
postoperative
death (unrelated
to an anastomotic
complication)
Ruiz-Tovar et al. Colon Right-sided colon Laparotomy Stapled (linear, CT scan - No bowel Wound infection, Intra-abdominal
(2012) [36] cancer and GIA80™; side- preparation; intra-abdominal abscesses: 5% in
elective surgery to-side/end-to- antibiotic infection, each group. Wound
end); handsewn prophylaxis anastomotic leak, infection: 10%
(2 layers; (metronidazole, hemorrhage, stapled, 7%
continuous; 3–0 tobramycin) operative time, handsewn.
polyglactyn; intra-abdominal Operative time:
side-to-side) abscess, 98.8 min stapled,
International Journal of Colorectal Disease

mortality, 105.2 min
hospital stay handsewn
(p = 0.013).
Positive cultures
were obtained in
79% of the cases
(2023) 38:52

after stapled
anastomosis and
73% after handsewn
 Table 2  (continued)
Source Site Procedure Surgical approach Characteristics of Diagnostic Other procedures Bowel Study endpoints Main results
anastomosis methods preparation and
prophylaxis

Zurbuchen et al. Colon Stenosing Laparotomy; Stapled (linear, Endoscopy - Anti-inflammatory Recurrence of Crohn’s disease
(2013) [37] ileitis terminalis laparoscopy; TA; side-to-side); prophylaxis Crohn’s disease, activity index:
in Crohn’s conversion handsewn (prednisolone, bleeding, wound 200.5 ± 73.66
disease who (interrupted, mesalazine, infection, side-to-side,
underwent an Gambe, 4–0 immunosuppres- anastomotic 219.6 ± 89.03 end-
ileocolic polyglactin); sive) leakage, first to-end.
resection continuous, postoperative Duration of surgery:
monofile; stool, hospital 126.7 ± 42.8 min
International Journal of Colorectal Disease

end-to-end) stay side-to-side,

137.4 ± 51.9 min
end-to-end.
Anastomotic
leakage: 6.5% end-
to-end. Impaired
(2023) 38:52

wound healing:
13.9% side-to-side,
6.5% end-to-
end. Hospital
stay: 9.9 ± 3.93,
10.4 ± 3.26 days
Bertani et al. Colorectal Radical colorectal Laparotomy; Stapled (end‐to‐ Radiography, Eight patients Enemas; MBP Surgical-site Surgical site
(2011) [38] resection for laparoscopy; end, termino‐ bacterial were not able to (polyethylene infection infection:
malignancy with robot lateral) examination, complete MBP glycol, hydro- (anastomotic 14.0% MBP,
primary surgery electrolyte leakage, wound 17.8% no-MBP
anastomosis infusion); infection, intra‐ (p = 0.475);
Intravenous abdominal Comparable in low
antibiotic abscess), extra‐ anterior
prophylaxis abdominal resection
(cefoxitin, infection and non‐ (p = 1.000),
metronidazole, infectious and minimally
gentamicin, complications, invasive procedure
clindamycin) hospital stay, (p = 0.241). No
postoperative perioperative
day of first bowel mortality
movement to gas,
mortality,
assessment of
response by
patients
undergoing
Page 13 of 24 

mechanical bowel
preparation and by
52

surgeons

13
 Table 2  (continued)
52  

Source Site Procedure Surgical approach Characteristics of Diagnostic Other procedures Bowel Study endpoints Main results
anastomosis methods preparation and

13
prophylaxis

Buchberg et al. Colorectal Left-sided Laparotomy; Compression (NiTi Air leak test, Additional purse MBP; Anastomotic Minor morbidities:
(2011) [18] colectomy and laparoscopy CAR™ 27, end- proctoscopic string suture Intravenous leakage, time to 13%, included one
Page 14 of 24

compression to-end) examination antibiotic return of bowel small

anastomosis with (flexible prophylaxis function, first postoperative
the CAR™ 27 sigmoidoscopy), postoperative abscess requiring
device direct toleration of antibiotics alone
palpation from liquids and and two
the abdominal solids, postoperative
side, surgery intraoperative anastomotic
device strictures requiring
failure, bleeding, balloon dilation.
stricture, wound Major morbidities:
infection, abscess 4%, included a
formation, partial anastomotic
peritonitis, dehiscence/leakage
readmission, requiring the
reoperation, surgical
death, length dismantling of the
of surgical anastomosis and
procedure, ring diversion
expulsion time,
and awareness
International Journal of Colorectal Disease
(2023) 38:52
International Journal of Colorectal Disease (2023) 38:52 Page 15 of 24  52

Table 3  Statistical analysis of the outcomes

Outcome Number of Number of Events per 100 patients or p I2(%) Chi-square
studies patients MRAW [95% CI] test (X2), p

Primary outcomes
  Dehiscence 16 6921 4.69 [3.56; 5.82] 0.81 63  < 0.01
  Mortality 12 6685 1.47 [0.75; 2.19] 0.78 77  < 0.01
  Reoperation 10 5255 6.84 [4.74; 8.95]  < 0.01 86  < 0.01
  Bleeding 10 4986 1.53 [0.57; 2.49] 0.73 0 0.65
  Stricture 6 549 2.52 [0.00; 5.25] 0.17 44 0.11
Secondary outcomes
  Wound infection 9 864 7.26 [4.71; 9.81] 0.31 35 0.12
  Intra-abdominal abscess 9 1216 1.74 [0.37; 3.11] 0.91 4 0.40
  Duration of surgery (minutes) 10 4897 146.80 [124.05; 169.54] 0.02 99  < 0.01
  Length of hospital stay (days) 14 6532 11.49 [9.42; 13.56] 0.56 99  < 0.01

Fig. 2  Forest plot of the proportion of dehiscence grouped by anastomotic technique (handsewn, stapled, or compression). Values are presented
as proportions with a 95% CI

13
 52   Page 16 of 24
technique is most effective in detecting anastomotic compli-
cations and which results should be considered. As shown,
only four studies compare different types of anastomosis and
none makes a global comparison of all techniques. For this
reason, this analysis covered not only comparative studies
but also studies evaluating isolated anastomotic techniques.
Techniques of colonic and rectal anastomosis
Each study was analyzed for the outcomes reported, with the
overall results shown in Table 2. Since the studies reported
different outcomes, each outcome was calculated for each
type of anastomosis, according to the number of patients in
the study who respond to it.
In the handsewn anastomosis, 146 patients of the 3513
presented dehiscences, 87 died in a total of 3482, 288 out of
3025 were reoperated, 2 out of 252 presented stricture, 36
out of 325 developed wound infection, 8 out of 416 presented
intra-abdominal abscess, and 49 showed bleeding in a total
Fig. 3  Forest plot of deaths per 100 patients grouped by anastomotic technique (handsewn, stapled, or compression). Values are presented as
proportions with a 95% CI
13
International Journal of Colorectal Disease (2023) 38:52
of 2815 patients. The mean duration of surgery was 139.92
(112.15–167.70) min in a total of 2937 patients. The mean
hospital stay was 13.20 (7.00–19.39) days in 3189 patients.
Regarding the stapled anastomosis, 164 out of the 3079
presented dehiscences, 79 in 2874 patients died, 179 out of
1960 were reoperated, 28 out of 1783 showed bleeding, 11
out of 185 presented stricture, 37 out of 476 developed wound
infection, and 10 out of 471 present intra-abdominal abscess.
The mean duration of surgery was 141.25 (105.55–176.94)
min in a total of 1897 patients. The mean hospital stay was
10.52 (8.58–12.46) days in 2242 patients.
Regarding compression anastomosis, 17 out of the 329
presented dehiscences, 3 patients died in a total of 329, 12
out of the 329 were reoperated, 8 out of the 329 presented
bleeding, 3 out of 112 presented stricture, 3 out of 63 devel-
oped wound infection, and 8 in the 329 presented intra-
abdominal abscess. The mean duration of surgery was 183.47
(163.90–203.04) min for a total of 63 patients. The mean of
hospital stay was 11.92 (9.30–14.54) days in 323 patients.
International Journal of Colorectal Disease (2023) 38:52 Page 17 of 24  52
Meta‑analysis of clinical outcomes
The overall pooled results of the primary and secondary
outcomes compared in this meta-analysis are summarized
in Table 3.
Primary outcomes
The dehiscence rate across all studies included in the quan-
titative analysis was 4.69 [3.56; 5.82]%. Subgroup analysis
showed no significant differences between anastomotic
techniques (p = 0.81) (Fig. 2). However, there is substantial
heterogeneity among the studies within the stapled group
( 𝜒10
2
= 47.82, p < 0.01, I = 79%). Sensitivity analysis was
performed by removing each study included in the meta-
analysis individually. This exclusion did not substantially
affect heterogeneity and had little effect on the statistical
analysis of dehiscence rate. Moreover, Egger’s test demon-
strated no publication bias (p = 0.28).
The mortality rate across all studies included in the
quantitative analysis was 1.47 [0.75; 2.19]%. Subgroup
analysis showed no significant differences between anasto-
motic technique groups (p = 0.78) (Fig. 3). However, there
Fig. 4  Forest plot of the proportion of reoperation grouped by anastomotic technique (handsewn, stapled, or compression). Values are presented
as proportions with a 95% CI
is substantial heterogeneity among the studies within the
handsewn and stapled anastomotic techniques ( 𝜒42 = 17.04,
p < 0.01, I = 77%; 𝜒62 = 39.72, p < 0.01, I = 85%, respec-
tively). Sensitivity analysis was performed by removing each
study included in the meta-analysis individually. The hetero-
geneity was substantially decreased in the handsewn group
after the exclusion of the Jurowich et al. [29] study. How-
ever, this change had little effect on the statistical analysis
of the mortality rate. Moreover, Egger’s test demonstrated
no publication bias (p = 0.21).
The reoperation rate across all studies included in the
quantitative analysis was 6.84 [4.74; 8.95]%. According to
Fig. 4, subgroup analysis showed significant differences
between anastomotic techniques (p < 0.01), with the com-
pression technique reporting the lowest reoperation rate
(3.64 [1.43; 5.84]%) and the handsewn the higher (9.49
[8.33; 10.64]%). However, there is substantial heterogene-
ity among the studies within the stapled group ( 𝜒52 = 52.93,
p < 0.01, I = 91%). Sensitivity analysis was performed by
removing each study included in the meta-analysis individu-
ally. The exclusion of each study did not substantially affect
heterogeneity and had little effect on the statistical analysis
13
 52   Page 18 of 24
of the reoperation rate. Moreover, Egger’s test demonstrated
no publication bias (p = 0.42).
The bleeding rate across all studies included in the quan-
titative analysis was 1.53 [0.57; 2.49]%. Subgroup analysis
showed no significant differences between anastomotic
techniques (p = 0.73) (Fig. 5). No significant heterogene-
ity among the studies was observed ( 𝜒12 2
= 9.64, p = 0.65,
I = 0%). Moreover, Egger’s test demonstrated no publication
bias (p = 0.61).
The stricture rate across all studies included in the quan-
titative analysis was 2.52 [0.00; 5.25]%. Moderate heteroge-
neity among the studies ( 𝜒52 = 9.00, p < 0.11, I = 44%) was
observed. Subgroup analysis showed no significant differ-
ences between anastomotic techniques (p = 0.17) (Fig. 6).
Sensitivity analysis was performed by removing each study
included in the meta-analysis individually. The heterogeneity
was substantially decreased after the exclusion of the Placer
et al. [33] study. However, this change had little effect on the
statistical analysis of proportion of stricture.
Fig. 5  Forest plot of the proportion of bleeding grouped by anastomotic technique (handsewn, stapled, or compression). Values are presented as
proportions with a 95% CI
13
International Journal of Colorectal Disease (2023) 38:52
Secondary outcomes
The wound infection rate across all studies included in the
quantitative analysis was 7.26 [4.71; 9.81]%. Subgroup anal-
ysis showed no significant differences between anastomotic
techniques (p = 0.31) (Fig.  7). Moderate heterogeneity
among the studies was observed ( 𝜒10 2
= 15.43, p = 0.12,
I = 35%). Sensitivity analysis was performed by removing
each study included in the meta-analysis individually. The
heterogeneity was substantially decreased after the exclusion
of the Herrle et al. [3] and Milone et al. [27] studies. How-
ever, this change had little effect on the statistical analysis of
wound infection rate. Moreover, Egger’s test demonstrated
no publication bias (p = 0.68).
The intra-abdominal abscess rate across all studies
included in the quantitative analysis was 1.74 [0.37; 3.11]%.
Subgroup analysis showed no significant differences between
anastomotic techniques (p = 0.91) (Fig. 8). Low heterogeneity
among the studies was observed ( 𝜒92 = 9.40, p = 0.40, I = 4%).
International Journal of Colorectal Disease (2023) 38:52 Page 19 of 24  52

Fig. 6  Forest plot of the proportion of stricture grouped by anastomotic technique (handsewn, stapled, or compression). Values are presented as
proportions with a 95% CI

Fig. 7  Forest plot of the proportion of wound infection grouped by anastomotic technique (handsewn, stapled, or compression). Values are pre-
sented as proportions with a 95% CI

13
 52   Page 20 of 24
Fig. 8  Forest plot of the proportion of intra-abdominal abscess grouped by anastomotic technique (handsewn, stapled, or compression). Values
are presented as proportions with a 95% CI
The mean duration of surgery across all studies included
in the quantitative analysis was 146.80 [124.05; 169.54]
min. According to Fig. 9, subgroup analysis showed signifi-
cant differences between anastomotic techniques (p = 0.02),
with the compression technique reporting the longer time to
perform the surgery (183.47 [163.90–203.04] min). How-
ever, there is substantial heterogeneity among the studies
within the stapled and handsewn groups ( 𝜒62 = 469.27,
p < 0.01, I = 99%; 𝜒32 = 235.68, p < 0.01, I = 99%, respec-
tively). Sensitivity analysis was performed by removing each
study included in the meta-analysis individually. The exclu-
sion of each study did not substantially affect heterogeneity
and had little effect on the statistical analysis of the duration
of surgery. Moreover, Egger’s test demonstrated no publica-
tion bias (p = 0.44).
The mean of hospital stay across all studies included in
the quantitative analysis was 11.49 [9.42; 13.56] days. Sub-
group analysis showed no significant differences between
anastomotic techniques (p = 0.56) (Fig. 10). However, there
is substantial heterogeneity among the studies within the sta-
pled and handsewn groups ( 𝜒82 = 694.71, p < 0.01, I = 99%;
𝜒42 = 439.85, p < 0.01, I = 99%, respectively). Sensitivity
analysis was performed by removing each study included in
the meta-analysis individually. The exclusion of each study
did not substantially affect heterogeneity and had little effect
13
International Journal of Colorectal Disease (2023) 38:52
on the statistical analysis of hospital stay. Moreover, Egger’s
test demonstrated no publication bias (p = 0.46).
Discussion
This systematic review and meta-analysis compares three
different anastomotic techniques, namely handsewn, stapled,
and compression, independently. Our analysis demonstrated
that, when a colonic and rectal surgery is performed, among
the wide variety of complications that may occur, the wound
infection showed a high prevalence (7.26% [4.71; 9.81]%),
followed by the need of reoperation and dehiscence. It was also
demonstrated no significant differences among handsewn,
stapled, and compression techniques regarding the occur-
rence of dehiscence, deaths, bleeding, stricture, wound infec-
tion, intra-abdominal abscess, and in the length of hospital
stay. However, differences were found regarding the reopera-
tion rates, with the handsewn technique reporting the highest
rate and the compression the lowest. Statistically significant
differences were also found in the time needed for surgery.
Regarding this outcome, the compression technique required
more time, being the handsewn the fastest technique.
Although the procedures of each technique differ, they are
quite similar concerning postoperative outcomes, and doubts
International Journal of Colorectal Disease (2023) 38:52 Page 21 of 24  52
Fig. 9  Forest plot of the mean duration of surgery grouped by anastomotic technique (handsewn, stapled, or compression). Values are presented
as means with a 95% CI
still exist regarding which procedure should be adopted. In
general, the literature also found no differences between the
techniques for most of the outcomes analyzed. Lustosa et al.
[39] did not found differences between the handsewn and sta-
pled techniques regarding mortality, dehiscence, hemorrhage,
reoperation, wound infection, and hospital stay. However, dif-
ferences were found in stricture with stapled technique report-
ing a higher incidence, and the handsewn technique requir-
ing more anastomotic time. MacRae et al. [20] also found
that stricture was more common in stapled technique than in
handsewn technique. Despite that, no differences were found
in mortality and clinical and radiologic leakage rates between
the two techniques. Likewise, Neutzling et al. [2] found no
significant differences between the handsewn and stapled
techniques regarding dehiscence rates, but also observed sig-
nificant stenosis in patients who underwent stapled anasto-
mosis comparing with handsewn. In turn, Slesser et al. [40]
compared compression with handsewn/stapled anastomosis
and did not find significant differences regarding mortality,
anastomotic leakage, stricture, length of surgery, and wound-
related, but a shorter postoperative stay was associated with
compression technique. Some authors [35, 41] reported that
in compression anastomosis, there is no retention of a for-
eign body at the anastomotic site and, therefore, a reduced
probability of late luminal narrowing. Other studies [9, 42]
reported that compression anastomosis is associated with
lower stricture rates when compared to other techniques. For
this reason, a lower incidence of wound infections should be
expected [35]. For others [20], the intraoperative technical
problems were more likely to occur with stapled than hand-
sewn anastomosis, but our results do not corroborate this
observation. Khromov et al. [35] demonstrated that compres-
sion technique presents anastomotic complications compara-
ble to the stapled. Kracht et al. [43] suggested that in stapled
anastomosis, there is less intra-operative septic contamination
since only small holes are opened to introduce the stapler;
whereas, in the handsewn anastomosis, the entire lumen of
the colon is exposed. Ruiz-Tovar et al. [36] consider that the
size of the opening of the lumen does not have a determining
role in peritoneal contamination. This may be greater in the
stapled anastomosis as a result of the fecal material that is
released when removing the stapler from the colon’s lumen,
but this finding was not observed in our results.
Taken together, our findings demonstrated that the com-
pression technique takes longer, but it can bring a better
prognosis in terms of future complications that lead to the
need of reoperation. However, possible study limitations may
affect the quality of the results obtained. The first limitation
13
 52   Page 22 of 24
Fig. 10  Forest plot of the mean of hospital stay grouped by anastomotic technique (handsewn, stapled, or compression). Values are presented as
means with a 95% CI
is related to the lack of direct comparison studies between
handsewn, stapled, and compression anastomosis. Thus, this
analysis included singular studies of each of the anastomotic
techniques, so that some types of variability in the definition
of outcomes, period of follow-up, and surgical procedures
may occur. Compression anastomosis was limited to the use
of a single device, and few studies still exist using this surgical
procedure. In addition, there is still a set of variables associ-
ated with clinical practice, ranging from different clinical con-
ditions of the patients, surgeons’ skills, type of surgery per-
formed, as well as anastomotic configurations. The duration
of the surgery is influenced by all surgical steps performed
and that may differ between studies and patients. Thus, ide-
ally, only the time required to perform the anastomosis would
be considered, but these data are scarce in the articles. For
the analysis of wound infection, data mentioning surgical site
infection were also excluded due to the impossibility to know
accurately whether it was a superficial infection restricted to
the wound site or not. The results obtained are still influenced
13
International Journal of Colorectal Disease (2023) 38:52
by the method used to diagnose complications, combined with
the personal interpretation that some cases may have. Fur-
thermore, certain characteristics of the studies can also have
their contribution, such as the existence or not of randomiza-
tion and the type of existing blind. All these study limitations
should be considered when adopting our findings to the clini-
cal practice.
Conclusions
The results obtained from this systematic review and meta-
analysis did not find sufficient evidences to conclude which
of the anastomotic techniques is more efficient and promotes
fewer postoperative complications. The differences found
were limited to the rate of reoperations, with compression
anastomosis reporting the lowest rate and the handsewn
anastomosis the highest. Despite this, surgeries with com-
pression anastomosis required more time, with the handsewn
International Journal of Colorectal Disease (2023) 38:52 Page 23 of 24  52
being the fastest technique. Therefore, it is not possible to
infer conclusions about which procedure is more appropriate
for anastomosis.
Acknowledgements  The authors thank the Portuguese Foundation for
Science and Technology (FCT) and CUF, S.A. for the PhD scholarships
of A. Oliveira (PD/BDE/142979/2018 and COVID/BDE/152779/2022).
Author contribution  Pedro Leão and Albino Martins had the idea for
the article; Ana Oliveira, Susana Faria, and Nuno Gonçalves performed
the literature search and data analysis; Ana Oliveira drafted the work;
Ana Oliveira, Susana Faria, Nuno Gonçalves, Albino Martins, and
Pedro Leão critically revised the work.
Funding  Open access funding provided by FCT|FCCN (b-on).
This work was also supported by National funds through the FCT-
UIDB/50026/2020 and UIDP/50026/2020 projects.
Data availability  The data analyzed in this study will be made available
upon reasonable request.
Declarations  10.​1111/j.​1463-​1318.​2004.​00657.x
Competing interests  The authors declare no competing interests.
Open Access  This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
tion, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article's Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
the article's Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/.
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