Seminars in Pediatric Surgery 27 (2018) 261–266

Contents lists available at ScienceDirect

Seminars in Pediatric Surgery

journal homepage: www.elsevier.com/locate/sempedsurg

Autologous intestinal reconstruction surgery

Gabriel Ramos-Gonzalez, Heung Bae Kim∗
Department of Surgery, Boston Children’s Hospital, 300 Longwood Avenue, Fegan 3 Boston, MA 02115, United States

a r t i c l e i n f o a b s t r a c t

Keywords: The management of short bowel syndrome has mainly been focused on intestinal rehabilitation as part
Autologous Intestinal Reconstruction of multidisciplinary team approach in specialized centers. While some patients go through a process of
Surgery
bowel adaptation that allows them to reach enteral autonomy, others reach a plateau before this and
Short Bowel Syndrome
require prolonged parenteral nutrition and/or intestinal transplantation. Various autologous intestinal re-
Parenteral Nutrition
Serial Transverse Enteroplasty construction procedures centered on bowel tapering have been described to increase functional intestinal
Longitudinal Intestinal Lengthening area and help gain enteral autonomy. This review discusses the surgical techniques, advantages, limita-
Intestinal Failure tions, and general outcomes of each procedure.
© 2018 Published by Elsevier Inc.

Introduction strives to optimize functional absorptive bowel area, while limiting

The introduction of parenteral nutrition (PN) to the clinical ar-
mamentarium in the late 1960s ushered in a new era in the care of
short bowel syndrome (SBS) and quickly became an essential com-
ponent in its management.1 However, PN-associated complications,
such as catheter-related infection/thrombosis and PN-associated
liver damage, represent the main cause of morbidity and mortal-
ity among SBS patients. While PN provides a temporary nutritional
solution and facilitates time for bowel adaptation, the long-term
management of SBS should be directed at minimizing the need for
PN.
Extensive surgical resection results in substantial loss of ente-
rocyte mass or functional mucosal surface that triggers the process
of bowel adaptation. On a macroscopic level this process results
in bowel dilation, which in turn results in dysmotility and ulti-
mately leads to stasis and bacterial overgrowth. On a microscopic
level, adaptation is associated with enterocyte proliferation, muscle
hypertrophy, increased villus height, and crypt depth.2 Theoreti-
cally, bowel adaptation progresses until enough functional mucosal
surface area has been restored so the patient can regain enteral
autonomy.3 Unfortunately, this is not always the case. Fig. 1 de-
tails the most common bowel adaptation scenarios in patients with
SBS and their theoretical response to various surgical management
options. Thus, autologous intestinal reconstruction surgery (AIRS)
Abbreviations: PN, parenteral nutrition; SBS, short bowel syndrome; AIRS, autol-
ogous intestinal reconstruction surgery; LILT, longitudinal intestinal lengthening and
tailoring; STEP, serial transverse enteroplasty; SILT, spiral intestinal lengthening and
tailoring.
∗
Corresponding author.
E-mail address: heung.kim@childrens.harvard.edu (H.B. Kim).
stasis and facilitating bowel motility.
Antiperistaltic or reversed intestinal segment surgery was
among the initial attempts at autologous reconstructive surgery.4,5
The proposed mechanism of action of a reversed segment is that
it should increase intestinal transit time and thus provide more
time for nutrient absorption. Unfortunately, this technique quickly
fell out of favor despite reports with up to 84% survival rates and
45% weaning from PN rate on 5-year follow-up due to technical
issues including a high rate of bowel obstruction.6 Colonic in-
terposition grafts,7,8 recirculating bowel loops,9 and nipple valve
construction10 are other techniques that have been proposed for
the management of SBS, but these are also prone to technical
complications and have all been disregarded. Recognizing the
contribution of intestinal dilation to the overarching problems of
malabsorption and motility in SBS patients, some authors focused
their efforts on developing intestinal tapering techniques based on
the excision or inversion of the redundant antimesenteric border
of the dilated intestine.11–13 These techniques have been almost
completely abandoned in favor of more recent procedures that
will be described in the following sections.
The overall management of SBS patients has largely become
centralized to large institutions with multidisciplinary care teams
focused on intestinal rehabilitation. While PN remains a mainstay
in the management of these patients, the goal of therapy is to di-
minish the need for PN and minimize its associated complications.
Although the role and timing of AIRS is a topic that continues to
be debated, we believe that it should be reserved for patients who
are unable to wean from PN after exhausting all available medi-
cal strategies.2 Hukkinen et.al reported that short remaining small
bowel segments, intestinal atresia etiology, and missing ileocecal
valve were independent risk factors for the tapering surgery in

https://doi.org/10.1053/j.sempedsurg.2018.08.001
1055-8586/© 2018 Published by Elsevier Inc.
262 G. Ramos-Gonzalez, H.B. Kim / Seminars in Pediatric Surgery 27 (2018) 261–266

Fig. 1. Theoretical bowel adaptation scenarios in short bowel syndrome patients. (A) Patient successfully weaned off PN after adequate bowel adaptation (B) Patient in which
bowel adaptation leads to bowel dilation, dysmotility and/or bacterial overgrowth might benefit from autologous intestinal reconstruction surgery (AIRS) such as the STEP
procedure to increase functional mucosal surface area (fMSA). (C) In patients who have insufficient actual mucosal surface area (aMSA) the only method to achieve full
enteral autonomy is through intestinal transplant. (D) Patient whose bowel redilates resulting in loss of fMSA and resumption of PN following initially successful AIRS may
be a candidate for repeat AIRS including the STEP procedure. [Reprinted with permission from Elsevier3 ].

children with SBS, while patients with SBS secondary to necro-
tizing enterocolitis were less likely to warrant tapering.14 On the
other hand, end-stage liver disease is now widely recognized as
a contraindication for AIRS, as these patients seem to gain more
benefit from transplantation.15,16
Longitudinal intestinal lengthening and tailoring (LILT)
Bianchi first described the longitudinal intestinal lengthen-
ing and tailoring (LILT) procedure in 1980 using a SBS porcine
model.17 The principle behind the LILT was to increase ex-
posure of the chyme to the intestinal mucosa and enhance
nutrient absorption by increasing bowel length and reducing
intestinal dilation. This procedure relies on the blunt dissection
of the mesentery into two leaves to create independent blood
supplies for the resulting segments of bowel. A surgical stapler
is then used to divide the dilated bowel in half along its longitu-
dinal axis through this mesenteric defect. After the entire length
of dilated bowel has been tailored and the two segments are
separated, they are anastomosed to one another in isoperistaltic
fashion [Fig. 2]. This groundbreaking procedure launched the era
of modern autologous intestinal reconstruction surgery.
Within a year of the first publication, the first human LILT pro-
cedure was described by Boeckman and Taylor in a 4-year-old boy
with short bowel syndrome due to gastroschisis and intra-uterine
volvulus.18 The patient had 50 cm of small bowel with dilation up
to 11 cm in some segments. Following a successful surgery, his fat
absorption coefficient increased from 35% to 50% and the patient
was weaned off PN 10 weeks later.
In 1984 Bianchi et.al reported a modified version of the proce-
dure in which the mesenteric and antimesenteric borders are di-
vided with electrocautery and the new segments re-approximated
using inverting Lembert sutures rather than using a surgical sta-
pler.19 While the author recognizes that either technique could be
used, he argues that the use of electrocautery and sutures poten-
tially reduces the risk of damage to the blood supply and inter-
loop fistulae. In another attempt to reduce potential post-surgical
complications, Chahine and Ricketts described a technical varia-
tion focused on reducing the number of anastomosis from three to
one.20 In their proposed modification, the stapling device is fired
obliquely at the proximal and distal ends of the small bowel to
keep the ends in continuity with the bowel.
Theoretically, the LILT procedure should result in a doubling
of the intestinal length and 50% reduction of intestinal diameter.
 G. Ramos-Gonzalez, H.B. Kim / Seminars in Pediatric Surgery 27 (2018) 261–266
Fig. 2. Longitudinal intestinal lengthening and tailoring technique. (A) Dissection
of the mesentery to create two peritoneal leaves. (B) View of the mesenteric border
with divided peritoneal leaves, each with independent blood supply. (C) Division
of dilated bowel longitudinally with surgical stapler to form two hemi-loops. (D)
Resulting hemi-loops of bowel with independent blood supply via corresponding
mesenteric leaf. (E) Isoperistaltic anastomosis of resulting two segments of bowel.
[Reprinted with permission from Elsevier17 ].
While the total intestinal surface area is preserved, the functional
absorptive capacity is increased secondary to the reduced dilation
and reduction of stasis due to intestinal dysmotility. One experi-
mental study demonstrated that animals that underwent the LILT
procedure had evidence of increased intestinal adaptation includ-
ing greater crypt depth and villus length compared to controls.21
Although LILT did not confer significant improvement with regards
to absorption, weight gain and nutritional status, it is likely that
the limited post-operative period was not enough to accurately re-
flect all benefits provided by the procedure.
The true benefit of AIRS relies on the ability to help wean pa-
tients from PN and avoid the devastating complications associated
to it. A review comprising 8 reports from the worldwide experi-
ence and including 150 patients who underwent LILT showed an
overall survival ranging between 30 and 100% with 28 and 100%
percent of survivors being able to be weaned to full enteral nu-
trition.22 Several additional large single-institution long-term out-
comes studies have been published since this review. Walker et.al
presented a series of 19 SBS patients with 79% overall survival and
60% intestinal transplantation rate among survivors with a me-
dian follow-up of 6.3 years. However, those who underwent LILT
but not transplantation had a 70% survival with a 9 year follow-
up, and 44% of patients weaned from PN did so with LILT pro-
cedure alone.23 Hosie et.al reported a 49-patient series with an
18% mortality rate and 39% patients weaned from PN at a mean
of 9 months; yet 40% of assumed survivors were lost to follow-
up.24 Khalil et.al reported an 89% survival post-LILT, with 87% of
263
survivors weaned off PN at a median time of 10 months.25 Fi-
nally, Reinshagen et.al published a 53-patients series with 77.4%
overall survival and a 79% enteral autonomy rate at a median 80
months follow-up.26 Length of the small intestine, length of large
intestine, pre-operative liver function and successful weaning from
PN within 18 months were significant prognostic factors related
to survival after LILT. The authors also reported that among pa-
tients presenting with elevated liver enzymes, weaning off PN after
LILT resulted in normalization of hepatic enzymes. On the contrary,
63% of those who remained PN-dependent persisted with elevated
enzymes.27
As with any surgical procedure, the LILT can result in proce-
dure specific post-surgical complications. One unique complication
that can develop following LILT is the potential necrosis of one of
the divided limbs as a result of compromised circulation to the
bowel segment.24,28 , 29 Other complications include: small bowel
obstruction secondary to adhesions, anastomotic strictures or leak-
age, d-lactic acidosis, interloop fistula, and recurrent bowel dilation
in the lengthened segment, recurrent abdominal pain and vomit-
ing, cholelithiasis, urolithiasis, and perianal eczema from increased
stool frequency.15,22 , 24,26 Regardless, sepsis and liver failure remain
the main causes of mortality after LILT.22,24 , 29
Iowa procedure
In the early 1990s Kimura et.al devised a new procedure based
on the concept that a segment of bowel could draw enough blood
supply from an adjacent structure in order to become fully inde-
pendent from the mesenteric circulation.30,31 The original rodent
model had an isolated jejunal segment with end fistulae and ex-
posed muscularis mucosa on the antimesenteric side following a
seromuscular incision. A corresponding incision was made in the
abdominal wall to expose the rectus abdominis muscle and these
two surfaces were brought together to create a myoenteropexy. Af-
ter detaching the mesentery from the bowel segment at various
time intervals, the investigators found that 7 weeks was adequate
to allow sufficient parasitization of blood flow from the abdominal
wall that the bowel segment could remain viable after complete
division of its mesenteric blood supply.
Additional experiments showed that the same principle of the
myoenteropexy could be successfully applied to other adjacent or-
gans in order to produce functional isolated bowel segments. The
Iowa II model focused on a hepatomyoenteropexy, while the Iowa
III model focused on an enteroenteropexy.32,33 These techniques
were first used in clinical care in 1993, as Kimura et.al reported the
use of a hepatomyoenteropexy to manage a 6-week-old with short
bowel syndrome due to intrauterine volvulus.34 After attaching a
dilated duodenal segment to the liver and allowing it’s antimesen-
teric border to gain independent blood flow for 16 weeks, a GIA
was used to divide the bowel horizontally similar to the LILT pro-
cedure. The antimesenteric border remained attached to the liver
as its blood supply, while the mesenteric side was anastomosed to
the distal portion of that segment in an isoperistaltic fashion.
This procedure was originally created as an alternative for the
LILT procedure in those patients who lacked a mobile mesentery
or those in whom the duodenum was involved. However, the com-
plexity of this surgery, the wait time required for parasitization
to occur and the need for multiple laparotomies has resulted in
limited adoption of this technique. Although there have been ad-
ditional reports using the Iowa procedure in the management of
short bowel syndrome, this technique has fallen out of favor and is
rarely reported in the current literature.
264 G. Ramos-Gonzalez, H.B. Kim / Seminars in Pediatric Surgery 27 (2018) 261–266
Fig. 3. Serial transverse enteroplasty technique. After creating a mesenteric window
(arrows), a GIA stapler is applied partially across and perpendicular to the longitu-
dinal axis of the bowel. This process is repeated throughout the dilated intestine
with stapler inserted from alternating sides, resulting in a zigzag shaped bowel lu-
men. [Reprinted with permission from Elsevier35 ].
Serial transverse enteroplasty (STEP)
In 2003, Kim et.al published the initial description of the serial
transverse enteroplasty (STEP) procedure in a porcine model.35 Six
pigs underwent laparotomy and reversal of a 55 cm jejunum seg-
ment in order to recreate the bowel dilation seen with the adap-
tive process of SBS. Five weeks later, animals were re-explored, the
reversed segment was excised, and bowel continuity restored. A
series of partial cuts were made using a GIA stapler alternating
from side to side in the dilated proximal bowel in order to create
a zigzag shaped bowel lumen [Fig. 3]. After six weeks, the animals
showed significant post-operative weight gain and a mean bowel
length increase of 64%.
The first human STEP procedure was subsequently reported by
Kim et.al36 that same year. The patient was a 2-year-old boy with
SBS secondary to gastroschisis and midgut volvulus who was un-
able to be weaned from PN despite being previously treated with
a LILT. At 23 months of age, one year after LILT, he underwent the
STEP procedure, in which an 83 cm segment of small bowel dilated
up to 6 cm in diameter was lengthened and tapered into a 147 cm
segment with a 2 cm diameter. At 6 months follow-up the patient
was able to wean to 50% enteral autonomy. Since that initial report
the STEP procedure has been adopted worldwide and used with
three primary indications: short bowel syndrome, intestinal atresia
with short residual bowel length37,38 and intractable D-lactic aci-
dosis secondary to bacterial overgrowth.39
The STEP procedure relies on the presence of intestinal dilata-
tion as part of the adaptive process in order to achieve intestinal
lengthening, yet not all patients present with sufficiently dilated
bowel to achieve adequate lengthening. In human patients the use
of reverse intestinal segments to cause proximal bowel dilatation,
as it is done in animal models, is not routinely performed due to
the high rate of potential complications. Recently, Wales et.al sug-
gested a protocol for the use of delayed STEP in children with con-
genital ultra-SBS (<20% predicted small bowel length) secondary to
vanishing gastroschisis or jejunal atresia.40 Following gastrostomy
placement, patients were allowed oral feeds along with intermit-
tent gastrostomy tube clamping trials. Serial upper gastrointestinal
studies were perform every 4 weeks until bowel caliber reached
5 cm, which occurred at a mean 116 days. This protocol resulted in
intestinal dilation allowing for adequate lengthening with the STEP,
although the true mechanism for the dilation remains unclear.
In the 15 years since the STEP procedure was originally de-
scribed, multiple single-center studies as well as two reports from
the International STEP registry have been published. These pa-
pers suggest that patients have an overall increase in bowel length
of approximately 38–91% following the STEP procedure.41–49 The
long-term outcomes of the STEP have been based on analysis of
the degree of enteral autonomy and transplant free-survival. In
2013 Jones et.al3 published the 6-year experience from the STEP
registry including 50 centers from over 13 countries. A total of
111 patients were in the registry but only 97 were included in
the analysis, with gastroschisis with or without volvulus being
the most common primary underlying diagnosis. Enteral autonomy
was reached by 47% of patients and was associated with longer
pre-STEP bowel length. There was an 89.6% (87/97) transplant-
free survival following the STEP procedure. A higher serum direct
bilirubin level and shorter pre-STEP bowel length were associated
with death or transplant on multivariate analysis.
A meta-analysis designed to determine the effect of STEP on
improving enteral autonomy in children with SBS determined that
87% of patients had an increase in enteral tolerance and mean per-
cent tolerance of enteral nutrition went from 35.1% to 69.5%.50 This
supports the findings from the first report of the STEP registry that
demonstrated an increased in enteral tolerance from 31 to 67%.49
Importantly, increased enteral tolerance has also been shown to be
associated with improved growth in SBS patients, who frequently
have very low height and weight percentiles.51
Post-surgical complications of the STEP include small bowel
obstruction, bowel re-dilatation, intra-abdominal abscess,
hematomas, anastomotic leakage and gastrointestinal bleed-
ing. The latter two have been associated with the use of surgical
stapling devices. In one of the first cases described, Gibbons et.al
reported a 6-year-old patient who developed anemia and heme
positive stools eight months post-STEP and was diagnosed with
multiple ulcerations near the staple line by capsule endoscopy.52
In a review of 23 patients who underwent STEP, 3 patients (13%)
experienced gastrointestinal hemorrhage requiring blood trans-
fusion, two of which were due to ulcers along the staple line.53
While most of these episodes resolve with medical manage-
ment, the need for embolization has been reported.54 In a recent
study, tissue fusion devices were successfully used to perform
the STEP procedure in four pigs.55 The use of these devices in
the STEP procedure might prove beneficial in the reduction of
post-surgical complications and cost, but there is not enough data
to recommend their use in human procedures at this time.
Recurrent dilation of the bowel following an intestinal length-
ening procedure is not an uncommon occurrence. In one study that
examined predictors of repeat STEP, the absence of ileocecal valve
was identified as the main risk factor.41 Bowel redilation has been
associated with decreased ability to wean off PN and increased
need for re-operation.56,57 In some cases a second STEP procedure
is necessary in order to manage post-STEP bowel. Once the feasi-
bility of a repeat STEP had been shown in a porcine model, Erlich
et al reported the first application of sequential STEP in a patient
in 2007.58,59 In the 2013 review of the STEP registry, 16% of the co-
hort required an additional STEP procedure.3 Multiple series have
shown that STEP following intestinal lengthening procedures can
further lengthen the intestine between 20 and 60% and wean from
parenteral nutrition in approximately 43%.44,60 , 61
There is now over 35 and 15 years of clinical experience with
the LILT and STEP procedures, respectively. This lengthy experience
has allowed for multiple long-term reports to be published and for
comparisons to be made between these procedures. A large single-
institution series by Sudan et.al established that STEP resulted in
 G. Ramos-Gonzalez, H.B. Kim / Seminars in Pediatric Surgery 27 (2018) 261–266
a significantly greater increase in bowel length, decreased need
for transplant, and a trend to improved weaning off PN; however
no difference in survival was observed between the procedures.29
King et.al and Frongia et.al published two systematic reviews com-
paring the outcomes between LILT and STEP.15,62 Both reviews fa-
vored the STEP as having less need for intestinal transplantation
and decreased mortality, although King et.al argues the difference
is non-significant if only LILT performed after 1996 are taken into
account. On the other hand, the LILT was associated with better
outcomes with regards to weaning patients from PN. King et.al es-
tablished an overall surgical complication incidence rate of 17% for
LILT and 26% for STEP. However, both authors agree that LILT had a
higher incidence of fistula, intestinal necrosis, and abscess; while
STEP had increased risk for bleeding and bowel redilation. Both
procedures seem to have comparable risk for obstruction and leak-
age. These reports should be interpreted within the context of their
limitation, which include the significant discrepancy in the poten-
tial follow-up times between procedures.
Spiral intestinal lengthening and tailoring (SILT)
The spiral intestinal lengthening and tailoring (SILT), origi-
nally proposed by Cserni et al, is a new technique in which full-
thickness spiral cuts are created on the dilated bowel which is then
stretched out and retubularised.63 Initial proof-of-concept with a
double layer bowel model simulator showed a proportional rela-
tionship between the angle of the spiral incisions and degree of
bowel lengthening and narrowing achieved (45° cuts: 60% length-
ening, 33% tailoring; 60° cuts: 73% lengthening, 44% tailoring). Fur-
ther experiments with porcine bowel showed that cuts between
45° and 60°, along with 5 cm mesenteric incisions where the spi-
ral cuts met the mesentery, yielded 136% lengthening and 56%
tailoring.
The first in vivo study used six Vietnamese minipigs and a
methodology similar to the initial STEP experiments to promote
bowel dilation. On post-operative week five the animals underwent
the SILT procedure with cuts between 45° and 60°. Five weeks
after that they were finally euthanized and re-explored to assess
bowel lengthening. The mean lengthening was 75% and mean ta-
pering 56%.64 Histologic analysis of the bowel showed hypertrophy
of the mucosa and muscle layer. Circular and longitudinal mus-
cle fiber orientation, along with neuroenteric structures were pre-
served. Two animals experienced a bowel obstruction, which was
attributed to extensive narrowing of the bowel lumen on retubu-
larisation. This problem was remedied by using a catheter as a
guide in later animals. A modified SILT technique was recently re-
ported by Mehrabi et.al in which the intestinal mucosa is left in-
tact.65 Although this was shown to be technically feasible, further
research and larger series are required to assess the true impact of
this technique.
In 2014, Cserni et.al first reported a 3-year-old girl with SBS
secondary to midgut volvulus who underwent successful bowel
lengthening using SILT.66 She only had 15 cm of jejunum, which
increased to 22 cm with a year of bowel expansion practices. By
using SILT with 45–60° cut angles it was possible to lengthen an
11 cm segment of dilated bowel into a 20 cm segment and taper
it around a catheter from 4 cm to 2 cm. Final overall bowel length
was 31 cm. No surgical complications occurred and the patient was
weaned off parenteral nutrition one-month post-SILT. At six-month
follow-up the operative segment appeared intact on imaging and
the patient continued off PN. A second case was reported in which
a neonate with massive bowel loss due to midgut volvulus who
underwent bowel expansion and successful SILT procedure to in-
crease intestinal length from 9 cm to 19 cm.67 At one year follow-
up the patient had reached over 80% enteral autonomy. Given the
265
lack of additional clinical data at this time the clinical significance
of this procedure remains unclear.
Conclusion
The management of SBS continues to progress and improve
over time. Care of these patients is increasingly performed at
specialized centers with multidisciplinary teams that can better
manage the complexities and challenges of this condition. Autol-
ogous reconstructive surgeries have been shown to be valuable ad-
juncts in the management of SBS that may allow select patients
to achieve full enteral autonomy and avoid the need for lifelong
PN or intestinal transplantation. The two most commonly used
procedures, the LILT and STEP, are both lengthening and tapering
procedures but the most important mechanisms of action is likely
related to the tapering effect which reduces problems associated
with bowel dilation including poor motility and bacterial over-
growth. These procedures should only be considered in the con-
text of a full multidisciplinary plan of care provided by a center
that specializes in intestinal rehabilitation.
Funding
This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
Conflict of interest
The author’s have nothing to disclose.
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