Early Human Development 97 (2016) 25–28

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Early Human Development

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

The surgical management of necrotising enterocolitis (NEC)

Hemanshoo Sudhir Thakkar 1, Kokila Lakhoo ⁎

Department of Paediatric Surgery, Oxford University Hospitals NHS Trust, Headley Way, Headington, Oxford OX3 9DU, United Kingdom

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

Article history: Necrotising enterocolitis (NEC) is a neonatal surgical emergency. At its early stages, the management of NEC is
Received 17 February 2016 largely medical using broad-spectrum antibiotics, gut rest and total parental nutrition. The only absolute indication
Accepted 1 March 2016 for surgery is an intra-abdominal perforation. There are several relative indications for surgery based on clinical,
biochemical and radiological parameters. Once the decision to intervene is made, several approaches may be
Keywords:
taken. Peritoneal lavage can be used as a salvage procedure or definitive management in some cases. The most
Necrotising enterocolitis
Perforation
common approach taken is bowel resection with enterostomy formation. There is a role for primary anastomosis
Peritoneal drain of bowel in limited NEC. In severe, multi-focal NEC a high diverting jejunostomy or “clip and drop technique” can
Peritoneal lavage be used. Laparoscopy has a limited role and is not widespread. The surgical complications of NEC include stoma
Enterostomy related morbidity, anastomotic leak/stricture and short-bowel syndrome. Long-term data on neurodevelopmental
Anastomosis outcomes is sparse but the present literature is suggestive of a negative impact in cases of surgically managed NEC.
Jejunostomy Crown Copyright © 2016 Published by Elsevier Ireland Ltd. All rights reserved.
Clip-and-drop
Laparoscopy
Neurodevelopmental

1. Introduction
Necrotising enterocolitis is the commonest neonatal surgical emer-
gency encountered by a paediatric surgeon [1]. The consequences of
this illness can be devastating and requires timely assessment and ac-
tion to reduce the morbidity and mortality associated with this condi-
tion. As has already been discussed, medical management can be
successful in treating NEC. Over the last few decades, advances in the
neonatal intensive care setting as well as availability of total parenteral
nutrition has certainly resulted in fewer infants requiring surgery [2].
However one third to one half of all diagnosed cases can lead to a com-
plication necessitating surgical intervention [1].
perforation. Risk factors identified in their series were persistent and
worsening pneumatosis on serial radiographic examination (Fig. 1),
sudden hyponatraemia, acidosis and a profound, sustained drop in the
platelet count suggestive of gangrene [2].
A recent study carried out in Michigan, USA attempted to identify
the optimal time for surgical intervention in a series of 197 infants [3].
Abdominal wall erythema, acidosis and hypotension were all indepen-
dently associated with surgical intervention. Table 1 summarises the
most common clinical, metabolic and radiological features universally
applied to identify at-risk infants.
3. Operative strategies

2. Indications for surgery
The commonest and only absolute indication for surgery in NEC is
a pneumoperitoneum secondary to intestinal perforation. There are
however relative indications for surgery which O′Neill et al. in
1975 first attempted discussed [2]. The authors raised the notion of
identifying the “at-risk” infant in whom early surgical intervention
may prevent progression to intestinal necrosis and subsequent
⁎ Corresponding author. Tel.: +44 1865 234197.
E-mail addresses: hemanshoo@gmail.com (H.S. Thakkar),
kokila.lakhoo@paediatrics.ox.ac.uk (K. Lakhoo).
1
Tel.: +44 1865 234197.
The surgical management of NEC has evolved over the last few
decades and several different approaches are now described in the
literature. The type of procedure employed is largely dictated by
the clinical condition of the patient as well the extent of bowel
affected.
The aims of surgery include:
1. Resecting gangrenous bowel or de-functioning it to reduce systemic
sepsis and subsequent risk of multi-organ failure
2. Early intervention to reduce degree of contamination and sepsis.
3. Preserving an adequate length of bowel to prevent short gut
syndrome.

http://dx.doi.org/10.1016/j.earlhumdev.2016.03.002
0378-3782/Crown Copyright © 2016 Published by Elsevier Ireland Ltd. All rights reserved.

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26 H.S. Thakkar, K. Lakhoo / Early Human Development 97 (2016) 25–28

90 day mortality. This study could not define the spontaneous perfora-
tion group (which is regarded as a separate disease) within the primary
drainage group thus the results need cautious interpretation. Also 40%
of the primary drainage group in this study required further laparotomy
and there were 3 further deaths in this group.
Several other studies were subsequently published in the literature
to confirm or refute these findings. In 2011, a Cochrane database sys-
tematic review was conducted analysing all randomised or quasi-
randomised controlled trials in preterm, low birth weight infants with
perforated NEC or spontaneous intestinal perforation [7]. Although
only two studies met the inclusion criteria (NECSTEPS and NET trials re-
spectively), again no significant difference was found between the two
groups in their survival at either 28 or 90 days.
In a recently conducted International survey at the European Paedi-
atric Surgeons' Association, 27% of respondents reported using primary
peritoneal drainage as definitive treatment for intestinal perforation in
extremely low birth weight infants [8]. 95% of UK surgeons also report
using peritoneal lavage as a stabilisation measures compared with 58%
for definitive treatment [9].

3.2. Bowel resection and enterostomy versus primary anastomosis

Fig. 1. Extensive pneumatosis in a terminally ill infant with NEC.
Each of the approaches discussed below involves a combination of
the above. There are risks and benefits to each. Although the final deci-
sion rests with the surgeon, the anaesthetist and neonatologist should
be closely involved in understanding the decision for surgery.
3.1. Peritoneal drainage versus laparotomy
The standard approach taken in infants who have perforated is to
perform a laparotomy. However, in those patients critically unwell
with respiratory compromise from abdominal distension and dia-
phragmatic splinting, primary peritoneal drainage can be performed
as a salvage procedure on the neonatal intensive care unit [4]. There
is, however, a controversy when the procedure is performed without
a subsequent formal laparotomy. Peritoneal drainage certainly pro-
vides a means of rapidly decompressing the abdomen, but it is also
believed that removing toxic effluents may promote spontaneous
healing. On the contrary, choosing not to excise necrotic bowel is
considered to be deleterious due to the ongoing cytokine and inflam-
matory response it can generate [5].
Moss et al. conducted a randomised controlled trial involving 117
preterm infants that were assigned to either primary peritoneal drain-
age or laparotomy for management of perforation [6]. No significant dif-
ference was found between the two groups in their primary outcome of
Once the decision to perform a laparotomy has been made, the tradi-
tional line of management is to resect necrotic bowel and subsequently
defunction the gut by fashioning a stoma (ileostomy and mucous fistula)
(Fig. 2). A widespread systemic inflammatory response and potential mi-
croscopic disease precluded earlier surgeons from considering an anasto-
mosis that may subsequently leak or stricture. However, stomal
complications including fluid/electrolyte imbalances, prolapse, retrac-
tion, skin excoriation/wound breakdown and the need for future reversal
surgery are strong arguments for considering a primary anastomosis.
Singh et al. performed a retrospective review comparing these two
approaches and found no significant difference in their complication
or mortality rate [10]. Similarly, Hall et al. reported comparable out-
comes in the two approaches even in infants weighing less than
1000 g [11]. These were not randomised control trials thus selection
bias need to be taken into account i.e. selection of primary anastomosis
for the more stable infant with limited disease.
At the same International Survey of the European Paediatric Sur-
geons' Association reported above, 67% of surgeons considered
performing an anastomosis in limited NEC disease whereas this figure
dropped to 15% when faced with multi-focal disease [8].
On balance primary anastomosis should be reserved for stable in-
fants with minimal abdominal faecal contamination.

Table 1
Clinical, metabolic and radiological features of an “at-risk” infant.

Clinical Metabolic Radiological

Abdominal wall erythema Thrombocytopaenia Fixed loop of bowel

Palpable abdominal mass
Hypotension
Metabolic acidosis Profound pneumatosis
Hyponatraemia Portal venous gas
Elevated C-reactive protein Pneumoperitoneum
(CRP)
Fig. 2. Clearly defined segments of NEC affected bowel.

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 H.S. Thakkar, K. Lakhoo / Early Human Development 97 (2016) 25–28
Fig. 3. Macroscopic appearance of multi-focal NEC.
3.3. Proximal diverting jejunostomy for severe necrotising enterocolitis
In the management of severe multi-focal NEC, bowel resection with
or without an anastomosis may predispose the infant to short gut syn-
drome (Fig. 3). (See Fig. 4.)
Furthermore, the infant may be too unstable to undergo a resection
or have a significant risk of major bleeding. In such cases, a proximal di-
verting jejunostomy can be fashioned as a salvage procedure to stabilise
the neonate. Recently a single institution reported their outcomes over a
10 year period amongst neonates undergoing this approach [12]. Two-
thirds of the 17 patients in this series had multi-focal disease, with the
remaining third having pan-intestinal NEC. 11 patients (65%) survived
to achieving enteral autonomy. The majority of infants who died had
pan-intestinal NEC and demised shortly after their surgery from
multi-organ failure. In cases of severe multi-focal NEC, 9% of European
surgeons would opt for a jejunostomy and this figure rises to 35% in
cases of pan-intestinal NEC [8]. This approach is hence certainly feasible
but does hold the risk of stoma related complications. In particular, fluid
and electrolyte loss can be troublesome in a jejunostomy and enteral
continuity should be sought after at the earliest opportunity.
3.4. “Clip and drop technique” for severe multi-focal necrotising
enterocolitis
This technique was first reported in 1996 and avoids an initial bowel
anastomosis or enterostomy. Usually applied to multi-focal NEC, gan-
grenous bowel segments are resected with the ends tied off using su-
tures. Bowel with questionable viability is usually retained and a re-
Fig. 4. Useful flow chart of surgical strategy for the management of NEC [15].
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27
look laparotomy performed 24–48 h later to determine the true extent
of the disease (Fig. 3). Any further segments affected can then be
resected again and a stoma +/− anastomosis can be performed. This
approach has the advantage of controlling the initial sepsis driven by
gangrenous bowel and avoiding unnecessary extensive bowel resection
predisposing the infant to short gut syndrome [13].
In 2012, Pang et al. reported their single-centre outcomes using this
technique [13]. The 30-day mortality for 16 patients undergoing this
procedure was 31.6%. Prior to this series, Ron et al. reported a 50%
long-term survival in their group of 13 infants with the same technique
[14]. Whereas the mortality using this technique is significant, it is usu-
ally employed in critically unwell infants with multi-focal disease inher-
ently predisposing them to a poor outcome. This approach nonetheless
is part of the armament of a paediatric surgeon when faced with a diffi-
cult presentation of NEC.
3.5. What is the role of laparoscopy in necrotising enterocolitis?
Smith and Thyoka conducted a systematic review of the literature
to answer the above question [16]. Seven studies were identified (6
case series and 1 case report) reporting the use of laparoscopy in
44 patients. Following the procedure, 8 (18%) infants did not require
any further surgery for reasons including a lack of evidence of NEC
and/or perforation as well NEC totalis. The remaining patients subse-
quently underwent either insertion of a drain, enterostomy or bowel
resection and anastomosis. There was only one case of a missed per-
foration at initial laparoscopy requiring a subsequent laparotomy.
The authors concluded that laparoscopy can be a useful tool in the
assessment of selected patients in whom further surgery may be
avoided.
Within Europe, less than 10% of surgeons report using this technique
[8]. In the majority of cases, effective laparoscopy will require the use of
carbon dioxide insufflation to create a pneumoperitoneum which may
negatively impact on the pathophysiology of these sick babies. Concerns
have also been raised from neonatal anaesthetists regarding the acid–
base instability of these infants undergoing laparoscopy. Careful patient
selection is required to ensure this can be safely performed. It can also
be argued that those patients who are subsequently deemed not to re-
quire any further surgery may have incorrectly been assessed in the
first place. Larger studies with prospective data are nonetheless re-
quired before laparoscopy becomes standardised as a surgical approach
in the management of NEC.
3.6. Surgical complications of NEC
3.6.1. Stoma related morbidity
The commonest complications of an enterostomy include fluid
and electrolyte losses, localised skin excoriation and stomal stenosis/
prolapse/relapse. Fluid losses can be particularly troublesome and
have a significant impact on the infant's growth. Twice weekly urinary
28 H.S. Thakkar, K. Lakhoo / Early Human Development 97 (2016) 25–28
sodium measurements and subsequent supplementation is thus recom-
mended. In some cases, early restoration of bowel continuity is the only
option to manage the encountered losses.
Prior to closure of the stoma, a contrast loopogram is performed
through the mucous fistula to check for the presence of any strictures
that can be excised during the same laparotomy.
3.6.2. Anastomotic complications
The two most commonly recognised complications are anastomotic
leak and anastomotic stricture. As has already been discussed, there is a
role for primary anastomosis in cases of limited NEC. In experienced
hands, the time taken for this should be comparable to that required
for an enterostomy. There is however again a lack of robust data demon-
strating the supremacy of one approach over the other. Outcome data
from the multicentre randomised controlled STAT trial is awaited to in-
form further discussion on this controversy [17].
3.7. Outcomes of surgically managed NEC
The overall mortality from NEC has reduced from 50% in the
1970s to be between 20 and 30% currently [14]. This is largely due
to advancements in neonatal intensive care as well increasing scien-
tific understanding of the pathophysiology of NEC. A recently pub-
lished retrospective review of outcomes in a UK tertiary centre
reported a 58% 30 day mortality. This cohort was however largely
consistent of extremely premature low birth weights in whom the
outcome is generally poor [18].
The short-term overall outcomes of each surgical approach have al-
ready been highlighted. There is however a paucity of data discussing
the long-term outcomes of this condition. In 2012, Pike et al. extended
the ORACLE study to analyse outcomes at 7-years of age for children
that had either proven or suspected NEC [19]. Data attained for 119 pa-
tients compared with infants without NEC. At 7 years of age, NEC con-
ferred an increased risk of both cognitive impairment as well as
generic bowel symptoms including stoma related complications. Rees
et al. also reported poor neurodevelopmental outcomes amongst in-
fants with more advanced disease and those treated surgically [20]. Fur-
ther long-term cognitive data up to 18–22 months of age is being
awaited from the “Laparotomy vs. Drainage for Infants with Necrotizing
Enterocolitis” (NEST) trial [17].
3.7.1. Key guidelines
• NEC is the commonest neonatal surgical emergency.
• The only absolute indication for surgery is a perforation.
• Lack of improvement despite optimal medical treatment is also indi-
cation to intervene.
• Clinical, biochemical and radiological features collectively inform the
assessment of a critically unwell neonate.
• Peritoneal drainage is considered by most as a salvage procedure only
whereas some have used it successfully as definitive management in a
specific group.
• There is a role for bowel resection and primary anastomosis in limited
NEC.
• An enterostomy is the usually preferred approach but should be
weighed up against the risks associated with a stoma.
• Severe NEC can be managed with a high proximal jejunostomy or
using the clip and drop technique.
• There is limited evidence on the role of laparoscopy in NEC.
• NEC is associated with significantly worse neurodevelopmental out-
comes beyond that can be attributed to prematurity.
3.7.2. Research directions
• The NEST trial will be assessing the effectiveness of laparotomy versus
peritoneal drainage in extremely low birth weight infants.
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• The STAT trial is an international, multicentre, prospective randomised
controlled trial comparing intestinal resection with stoma formation
or intestinal resection with primary anastomosis in the surgical man-
agement of neonates with necrotizing enterocolitis (NEC).
• The British Association of Paediatric Surgeons Congenital Anoma-
lies Surveillance System (BAPS-CASS) has completed a national
audit on NEC outcomes. The results of this study are due to be
published.
Conflict of interest statement
The authors declare that they have no conflict of interest, financial or
otherwise, relating to this article.
References
[1] M.C. Henry, Moss R. Lawrence, Surgical therapy for necrotizing enterocolitis: bring-
ing evidence to the bedside, Semin Pediatr Surg 14 (3) (2005) 180–190.
[2] J.A. O'Neill Jr., M.T. Stahlman, H.C. Meng, Necrotizing enterocolitis in the newborn:
operative indications, Ann Surg 182 (3) (1975) 274–279.
[3] A.J. Munaco, M.A. Veenstra, E. Brownie, L.A. Danielson, K.B. Nagappala, M.D. Klein,
Timing of optimal surgical intervention for neonates with necrotizing enterocolitis,
Am Surg 81 (5) (2015) 438–443.
[4] S.H. Ein, D.G. Marshall, D. Girvan, Peritoneal drainage under local anesthesia for per-
forations from necrotizing enterocolitis, J Pediatr Surg 12 (1977) 963–967.
[5] A. Rakshasbhuvankar, S. Rao, C. Minutillo, I. Gollow, S. Kolar, Peritoneal drainage
versus laparotomy for perforated necrotising enterocolitis or spontaneous intestinal
perforation: a retrospective cohort study, J Paediatr Child Health 48 (3) (2012)
228–234.
[6] R.L. Moss, R.A. Dimmitt, D.C. Barnhart, et al., Laparotomy versus peritoneal drainage
for necrotizing enterocolitis and perforation, N Engl J Med 354 (21) (2006)
2225–2234.
[7] S.C. Rao, L. Basani, K. Simmer, N. Samnakay, G. Deshpande, Peritoneal drainage ver-
sus laparotomy as initial surgical treatment for perforated necrotizing enterocolitis
or spontaneous intestinal perforation in preterm low birth weight infants, Cochrane
Database Syst Rev 15 (6) (2011).
[8] A. Zani, S. Eaton, P. Puri, et al., International survey on the management of necrotiz-
ing enterocolitis, Eur J Pediatr Surg 25 (1) (2015) 27–33.
[9] C.M. Rees, N.J. Hall, S. Eaton, A. Pierro, Surgical strategies for necrotising enterocoli-
tis: a survey of practice in the United Kingdom, Arch Dis Child Fetal Neonatal Ed 90
(2) (2005) 152–155.
[10] M. Singh, A. Owen, S. Gull, A. Morabito, A. Bianchi, Surgery for intestinal perforation
in preterm neonates: anastomosis vs stoma, J Pediatr Surg 41 (4) (2006) 725–729.
[11] N.J. Hall, J. Curry, D.P. Drake, L. Spitz, E.M. Kiely, A. Pierro, Resection and primary
anastomosis is a valid surgical option for infants with necrotizing enterocolitis
who weigh less than 1000 g, Arch Surg 140 (12) (2005) 1149–1151.
[12] M. Thyoka, S. Eaton, E.M. Kiely, Outcomes of diverting jejunostomy for severe nec-
rotizing enterocolitis, J Pediatr Surg 46 (6) (2011) 1041–1044.
[13] K.K. Pang, N.S. Chao, B.P. Wong, M.W. Leung, K.K. Liu, The clip and drop back tech-
nique in the management of multifocal necrotizing enterocolitis: a single centre ex-
perience, Eur J Pediatr Surg 22 (1) (2012) 85–90.
[14] O. Ron, M. Davenport, S. Patel, et al., Outcomes of the “clip and drop” technique for
multifocal necrotizing enterocolitis, J Pediatr Surg 44 (4) (2009) 749–754.
[15] A. Pierro, N. Hall, Surgical treatment of infants with necrotizing enterocolitis, Semin
Neonatol 8 (3) (2003) 223–232.
[16] J. Smith, M. Thyoka, What role does laparoscopy play in the diagnosis and immedi-
ate treatment of infants with necrotizing enterocolitis? J Laparoendosc Adv Surg
Tech A 23 (4) (2013) 397–401.
[17] M.V. Raval, N.J. Hall, A. Pierro, R.L. Moss, Evidence-based prevention and surgical
treatment of necrotizing enterocolitis-a review of randomized controlled trials,
Semin Pediatr Surg 22 (2) (2013) 117–121.
[18] K. Lakhoo, R.D. Morgan, H.S. Thakkar, et al., Exploratory laparotomy in the manage-
ment of confirmed necrotizing enterocolitis, Ann Pediatr Surg 11 (2) (2015)
123–126.
[19] K. Pike, P. Brocklehurst, D. Jones, Outcomes at 7 years for babies who developed neo-
natal necrotising enterocolitis: the ORACLE Children Study, Arch Dis Child Fetal Neo-
natal Ed 97 (5) (2012) F318–F322.
[20] C.M. Rees, A. Pierro, S. Eaton, Neurodevelopmental outcomes of neonates with med-
ically and surgically treated necrotizing enterocolitis, Arch Dis Child Fetal Neonatal
Ed 92 (3) (2007) F193–F198.