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Accepted Manuscript
Open Abdomen with Concomitant Entero-Atmospheric Fistula: Attempt to Rationalize
the Approach to a Surgical Nightmare and Proposal of a Clinical Algorithm
Salomone Di Saverio , MD, Antonio Tarasconi , MD., Kenji Inaba , MD, FACS,
Pradeep Navsaria , MBChB, FCS(SA), FACS, Federico Coccolini , MD, David Costa
Navarro , MD, Matteo Mandrioli , Panteleimon Vassiliu , MD, FACS, Elio Jovine , MD,
Fausto Catena , MD, Gregorio Tugnoli , MD
PII: S1072-7515(14)01845-6
DOI: 10.1016/j.jamcollsurg.2014.11.020
Reference: ACS 7650
To appear in: Journal of the American College of Surgeons
Received Date: 5 September 2014
Revised Date: 8 November 2014
Accepted Date: 12 November 2014
Please cite this article as: Di Saverio S, Tarasconi A, Inaba K, Navsaria P, Coccolini F, Navarro
DC, Mandrioli M, Vassiliu P, Jovine E, Catena F, Tugnoli G, Open Abdomen with Concomitant
Entero-Atmospheric Fistula: Attempt to Rationalize the Approach to a Surgical Nightmare and
Proposal of a Clinical Algorithm, Journal of the American College of Surgeons (2014), doi: 10.1016/
j.jamcollsurg.2014.11.020.
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Open Abdomen with Concomitant Entero-Atmospheric Fistula: Attempt to Rationalize the
Approach to a Surgical Nightmare and Proposal of a Clinical Algorithm
Salomone Di Saverio, MD (1), Antonio Tarasconi, MD. (2), Kenji Inaba, MD, FACS (3), Pradeep
Navsaria, MBChB, FCS(SA), FACS (4), Federico Coccolini, MD (5), David Costa Navarro, MD (6),
Matteo Mandrioli (1), Panteleimon Vassiliu, MD, FACS (7), Elio Jovine, MD (1), Fausto Catena,
MD (2), Gregorio Tugnoli, MD (1),
(1) Maggiore Hospital – Bologna Local Health District, and Emergency Surgery and Trauma
Surgery Unit, Maggiore Hospital Trauma Center, Bologna, Italy.
(2) Department of Emergency and Trauma Surgery - Maggiore Hospital, Parma, ITALY
(3) Department of Surgery. University of Southern California, Los Angeles, USA
(4) Trauma Center, Groote Schuur Hospital & University of Cape Town, South Africa
(5) General and Emergency and Trauma Surgery, Hospital Papa Giovanni XXIII, Bergamo, Italy
(6) Department of Surgery, Alicante University General Hospital, Alicante, Spain
(7) Attikon University Hospital, Department of Surgery IV, Surgery and Traumatology, Athens,
Greece
Disclosure Information: Nothing to disclose.
Technique partially presented at the video session, 98th
Clinical Congress of the American College
of Surgeons, Chicago, IL, October 2012. Management Algorithm presented at the
International Trauma & Emergency Surgery Week, Alicante, Spain, June 2014.
Correspondence address:
Salomone Di Saverio, MD
Maggiore Hospital, L.go Nigrisoli 2, Bologna Italy
Fax: +390516478412
email: salo75@inwind.it
Brief title: Entero-Atmospheric Fistula Management
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Abbreviations and Acronyms
AAST = American Association for the Surgery of Trauma
EAF = entero-atmospheric fistula
ECF = entero-cutaneous fistula
IAS = intra-abdominal sepsis
NPWT = negative pressure wound therapy
POD = post-operative day
The development of an entero-atmospheric fistula (EAF) in the midst of an open abdomen
represents a surgical nightmare, with an extremely challenging critical care problem set including
the full spectrum of surgical, metabolic, nutritional and nursing issues. Spontaneous closure is rare
as there is no fistula tract and there is a lack of well vascularized overlying tissue. For these reasons,
the acute fistula management should aim to completely divert fistula output, protect the surrounding
viscera and allow for the granulation of exposed bowel. This is difficult to achieve, because of the
extreme frailty of the surrounding tissues, which are chronically injured by enteric fluids, and the
multiple systemic derangements of the patient, driven by severe dehydration, electrolyte and
acid/base disturbances, a hypercatabolic status and ongoing sepsis. Despite the advancements in
critical care and surgical management, EAF-related mortality is still upwards of 40%[1]
.
Significant heterogeneity in the surgical techniques described for EAF management remains
and there is no single approach that has proven to be ideal in every circumstance: the aim of this
study is to develop a flowchart designed to help guide the surgeons who are caring for this
devastating complication, to choose the best approach on a case-by-case basis.
EAF definition, etiology and management
Entero-atmospheric fistula is defined as the occurrence of an enteric fistula in the middle of an open
abdomen. Specific characteristics defining EAF are: the absence of a fistula tract, the lack of well-
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vascularized surrounding tissue and location within an open abdomen, resulting in spillage of
enteric content directly into the open peritoneal cavity.
Little is known about the risk factors associated with EAF development. A recent
multicenter prospective observational study by Bradley, et al.[2]
has attempted to determine
independent predictors for the development of entero-cutaneous fistula (ECF), entero-atmospheric
fistula and abdominal sepsis (IAS) in patients undergoing damage control laparotomy after trauma.
Using the AAST (American Association for the Surgery of Trauma) Open Abdomen registry they
identified patients who developed ECF, EAF or IAS during open abdomen management following
damage control laparotomy and they compared the groups of patients with and without
complications. Interestingly, their data showed that large bowel resection, large volume
resuscitation and an increasing number of re-explorations were statistically significant predictors for
the development of a fistula within an open abdomen after trauma.
Another recent review of the available techniques for open abdomen management found a
higher incidence of EAF occurring in septic OA compared to non-septic OA (12.1% versus 3.7%
respectively). Furthermore, this review did not show any evidence of a relationship between use of
NPWT (Negative Pressure Wound Therapy) and fistula formation[3]
.For many years the application
of negative pressure has been considered the primary cause of fistula formation, but further studies
have demonstrated that fistula formation rate can be as low as 5%[4,5]
, even with a hand-made
dressing, and that in a good proportion of cases the fistula can spontaneously heal during NPWT[6]
.
In a recent relatively large series of EAF in patients treated with an OA for the management of
abdominal sepsis, the incidence of EAF was 54.5% (18/33)[7]
. In this series the rate of spontaneous
closure with NPWT was 22% (4/18). The average hospital stay was 88.89 days, the median number
of VAC (Vacuum Assisted Closure) applications was 22.5, and the median duration of VAC
applications 43.6 days. Mortality was as high as 44.4% (8/18).
Many of the principles applied to ECF management can be also considered in the
management of the EAF. The latter however are often more difficult as the unprotected bowel is
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friable and located within a “frozen abdomen”, precluding any possible surgical manoeuvres or
resection, with the added burden of peritonitis/sepsis due to the bowel content pooling directly
within the exposed peritoneal cavity.
Although the optimal option would be to perform a bowel resection or at least a proximal
bowel diversion, this option is invariably not feasible for multiple reasons including mesenteric
retraction and edema, the “frozen abdomen” and loss of domain due to retraction of the abdominal
wall.
As bowel resection or proximal diversion is not feasible, EAF management should aim to[8-10]
:
• decrease fistula effluent: the use of total parenteral nutrition, somatostatin and its
analogues[11-14]
as well as a proton pump inhibitor[15]
can be effective in decreasing the
bowel effluent;
• correct any fluid and electrolyte imbalances, acid/base derangements and reversal of the
hypercatabolic state (collection, quantification and characterization of bowel effluent are of
key importance);
• interrupt or prevent ongoing sepsis;
• divert fistula output, thus allowing granulation of the exposed bowel;
• if fistula closure is impossible, allow fistula to become chronic and controlled.
The goal should be to control and limit the acute phase of care. Fistula takedown and abdominal
wall reconstruction should be delayed optimally by at least 8 – 12 months, in order to allow
loosening of the visceral adhesions, and should be performed only when the patient is well
nourished and satisfactory physiological homeostasis has been achieved. Different methods for
definitive fistula takedown and bowel reconstruction are currently described in the literature[16-20]
.
Techniques for fistula effluent diversion
A wide spectrum of treatment options for effluent diversion has been described in the literature and
is often used at the discretion of the attending surgeon, as a universally accepted management
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algorithm does not exist. The following techniques can be individualized to patients depending on
their particular characteristics.
1. Negative Pressure Wound Therapy (NPWT)– The use of negative pressure in the open
abdomen with hand-made dressings is well described and some authors extended this
technique to cases of EAF. This method is the easiest to apply and represents the foundation
for many of the subsequent techniques.
2. Biological dressing / Fibrin Glue or Cyanoacrylates / Primary Suture[21,22]
–The application
of biological dressings (ie, Human Acellular Dermal Matrix or Cadaveric Split-thickness
Skin Graft) has been described with good results, particularly in case of a small size fistula
or deserosalization. Fibrin glue can improve the outcome of biological dressings, helping to
keep them in place and effectively sealing the fistula. Cyanoacrylates may be beneficial for
small EAFs, especially as an adjunct to primary suturing.[23]
3. Floating Stoma[24]
–This is made with a plastic silo placed over the open abdomen, where
openings are created to best fit the fistula opening; the edge of these openings are then
sutured to the margins of the opening in the enteric loops with a continuous polypropylene
suture. A stoma bag is then placed over this “floating stoma” in order to collect the enteric
effluent.
4. Fistula VAC[25]
–This method is easy and quick to apply, consisting of a single sheet of
Xeroform dressing placed to protect the wound bed, with a hole cut for the enteric opening.
The VAC sponge is accurately tailored to fit the wound and to match the fistula opening,
and is placed over the Xeroform layer. An adherent polyurethane drape is eventually placed
over the sponge and a hole is cut in this drape directly over the fistula, to allow placement of
the appliance of an ostomy bag for collecting the fistula effluent. A number of refinements
to this technique are described in literature, all attempting to obtain a better sealing of fistula
area from the rest of the wound[26-28]
.
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5. Tube VAC[29]
–The EAF is intubated with Malecot catheters and the surface of the open
abdomen is covered with petroleum-impregnated gauge. The wound is then covered with a
polyurethane sponge and the Malecot catheters are pulled through it. The entire device is
then sealed with an occlusive dressing and a continuous negative pressure is applied.
6. Baby Bottle Nipple VAC[30-38]
–A baby bottle rubber nipple is placed over the fistula opening
and a Pezzer tube, Malecot or Foley catheter is placed through a small hole cut into the tip
of the nipple. A round layer of colostomy paste can be placed under the nipple in order to
ensure a better seal. A petroleum jelly-impregnated gauge or clear Telfa sheet is then placed
over the bowel and the entire wound is covered by a commercial VAC dressing. A small
hole is shaped into the VAC sponge, to hold the nipple in place.
7. VAC Chimney[31]
– A chimney is created with a white sponge dressing, with the base of this
construct covering the adjacent healthy tissue for an area of 2-3 cm, to avoid leakage of
bowel effluent. A plastic tube, shorter than the chimney, is then placed into the chimney
itself, to avoid its collapse. The open abdomen is then covered with a conventional VAC
dressing, placing the connector to the pump directly over the chimney.
8. Fistula Patch[32]
– A soft, flexible gel lamellar is shaped into a round form. Sutures are then
placed through the center of this circle and fixed to a drain tube placed across the fistula,
outside of the bowel. The silica gel lamellar is then folded and pushed into the fistula. Once
inside the bowel it will unwrap, acting like a patch inside the bowel. The fistula patch would
then remain in situ until the definitive fistula takedown operation. Some authors have
recently described a similar technique using a patch of hydrophilic polyvinyl alcohol foam
to cover small fistulas, combined with NPWT used on the remaining abdominal surface4
.
9. Fistula Plug[33]
– Thisisa plug designed to seal the EAF from inside consisting ofa circular
disk of 1mm thick silicone with a diameter of 2-5 cm. A Vicryl suture is passed through the
center of the silicon circle and then tied to a rubber band, with a bridge of foam-covered
aluminium. The silicone plug is then rolled and inserted into the fistula hole, the plug is
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hung on the bridge by means of the suspension suture and rubber band. The bridge is fixed
to the abdominal wall using a self-adhesive plaster. Eventually, when the fistula is closed,
the tread will be cut off and the silicon plug will be discharged at the time of defecation.
10. Pedicled flap– Different types of flaps have been described in the literature[18,34-36]
. Although
feasible and possibly effective, they are highly technically demanding and require a well-
stabilized patient, without ongoing sepsis or physiological derangements. For these reasons,
flaps remain a good option for definitive management, after the acute phase has resolved.
11. Suspension / Stoma Conversion[36,37]
– In selected cases, when the fistula is located near to
the edge of the abdominal wound, the fistula edges can be gently mobilized and tacked to
the lateral aspect of the dermis. This allows the fistula to maturate into a definitive ostomy,
while negative pressure is applied to the granulating open abdomen, which is now protected
from bowel effluent.
The pros and cons, estimated cost and technical difficulty of every approach are summarized in
Table 1. Costs have been estimated, because the prices of every device and surgical item vary
widely between different countries and hospitals. A NPWT device rental price of 997,50 € was
utilized for the estimates.
Baby Bottle Nipple Diversion – Description of the technique
We have developed a refinement[38]
of the technique previously described by Layton[30]
et al.,
improving what we have found to be the practical downsides of this interesting management option
for an EAF. This has been named the baby bottle nipple diversion. First, the fistula is exteriorized
as much as possible outside the abdominal cavity, thus creating a flat surface that will allow optimal
nipple placement. At this time, irrigation and exploration of the abdominal cavity should be
performed, to reduce peritoneal contamination and decrease ongoing sepsis.
After these preliminary steps, a baby bottle nipple of soft silicone is placed over the fistula
(Video 1). The tip of the nipple is cut and a small size Pezzer tube is pulled through the hole of the
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rubber nipple and secured in place by non-absorbable stitch tied around the tip of the nipple (Video
1). In order to achieve a better seal, an underlying layer of colostomy paste (Figure 1) can be placed
around the fistula and under the nipple, which is then surrounded by a jelly gauze, covering the
bowel and excluding the area of the fistula. We have modified Layton’s technique to further
optimize the external diversion of the fistula and minimize nipple dislocation by inserting a small
(10 Fr) Foley catheter (Figure 2) into the fistula opening and inflating the balloon gently with 2 to 3
cc of water. The Foley catheter is then passed through and secured to the silicone nipple neck.
Finally a NPWT dressing system is placed over the exposed viscera to promote surface
granulation (Video 1: Renasys™, Smith & Nephew Corporate). The plastic drape is placed over the
open abdomen and the nipple–tube complex is passed through a hole shaped within the drape and
the sponge. The plastic drape is then used to cover the sponge and shaped around the Pezzer tube.
The negative pressure is used to compress the dressing, hold the nipple in place and sealoff the
fistula (see Figure 3)
The baby bottle nipple diversion has the advantage of being effective even in cases of large, high
output fistulae and, unlike other techniques, can also be effective in case of multiple fistulae.
Clinical validation, patient 1
In October 2010 we applied this novel approach to the case of a 46-yearold male admitted for
complete adhesive small bowel obstruction and strangulation of a parastomal hernia, who
developed on postoperative day 7 two ileal perforations within a completely frozen abdomen.
These were initially treated with fibrin glue and an open abdomen with BogotĂĄ Bag. After 6 days of
NPWT therapy, a leak from one of the previously repaired perforations appeared. A further attempt
at direct repair with Vicryl stitches and fibrin glue was not successful and the baby bottle nipple
diversion was utilized.
After three months of treatment with NPWT and baby bottle nipple diversion, the fistula
output was diverted, effectively functioning as an ileostomy. The abdominal surface was almost
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completely covered by skin and subcutaneous tissue granulating from the edges of the abdominal
wall (Video 2 – CT scan); the patient was therefore discharged to a rehabilitation facility. After
three year follow-up, (Figure 4a, Figure 4b, Figure 4c) the patient has returned to a normal active
life with good quality of life. The previous EAF is functioning well as a natural ileostomy. The
open abdomen has evolved into a large herniation of intra-abdominal organs and only a thin skin
layer is covering the viscera (Figure 5 – three years follow-up CT scan).
Clinical validation, patient 2
In June 2013 we had to face a similar surgical nightmare: a 73-yearold male was admitted for acute
bleeding from multiple angiodysplastic foci and underwent emergent right colonic resection.
On POD #7 the hospital course was complicated by evisceration and ileal non-anastomotic
perforation. This was treated with ileal resection and primary anastomosis. Later on, the patient
underwent two subsequent re-laparotomies for evisceration and small bowel perforations. This was
further complicated by a massive abdominal wall necrotizing fascitis, which caused a great loss of
tissue within the abdominal wall and required NPWT dressing.
After 32 days and 14 NPWT dressing changes, two ileal EAF appeared within a few centimeters
from each other. At this point the abdomen was frozen and completely inaccessible, due to heavy
matted adhesions. Based on the satisfactory results of our previous experience, the Baby bottle
nipple diversion technique was utilized, even in the presence of these multiple fistulas (Video 3).
Two separate baby bottle nipples were placed over the fistulae, allowing effective and separate
isolation of the two different EAFs (Figure 3). After four dressing changes, both fistulae were well
controlled and both their size and output had strongly decreased. The surrounding viscera were
covered with Renasys™ dressing, (Smith & Nephew Corporate) and treated with low pressure (-60
to -80 mmHg) NPWT. In the absence of significant enteric contamination, a clean granulation bed
was formed.
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On POD #65, the patient died of acute pulmonary edema, secondary to myocardial infarction. At
this stage, the fistulae were well controlled and the abdomen was clean and rapidly granulating
(Figure 6).
Our proposal
The management of an EAF is extremely challenging and should be tailored to the specific
characteristics of each case. We believe that a systematic approach to the management of this
devastating problem is required. Therefore, after performing a comprehensive review of the
literature and analyzing the different options for EAF management, we have developed a flowchart,
merging all the techniques described to date and including our experience and techniques (Figure
7). This is one rational, practical method for approaching this surgical challenge.
The acute management of an EAF should aim to: 1) divert the fistula output, thus preventing the
spreading of intestinal fluid into the peritoneal cavity; 2) collect and quantify the fistula output, in
order to address and correct fluids and electrolyte imbalances; 3) protect and keep clean the
surrounding granulating viscera.
A thorough classification of EAF is essential for choosing the correct approach. According to the
literature, an EAF can be classified based on anatomic location (proximal/distal); fistula output
volume (low/moderate/high) and location in the open abdomen (superficial/deep) [10,16,39]
(Table 2).
It is well known that distal and low-output fistulas have a higher spontaneous closure rate than
those that are more proximal and with high-output. For this reason, in the case of de-serozalisation
and distal, small or low output fistulas, a first attempt at primary closure with sutures and sealants
(fibrin glue, cyanoacrylates)[21,23]
should be made. If this first attempt fails, the fistula must be
approached in the same manner as a proximal, large or moderate/high output fistulae.
The latter fistulae type is very unlikely to close with a glue/suture approach. The presence of
ongoing peritonitis should be the factor that drives the choice of the management technique.
Biologic dressings and flaps or skin grafting should be avoided in these cases with ongoing
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uncontrolled peritonitis, because of the high probability of failure (ie, graft rejection, flap necrosis
and lack of sepsis control).
If there is ongoing peritonitis, the primary aim of treatment should be the diversion of fistula
output, allowing improvement of the physiological condition of the patient.
In the most recent review on the management of EAF4
, Tavusbay et al. proposed different
techniques according to the size/output of the fistula. Small fistulae are first covered with a patch of
hydrophilic polyvinyl alcohol foam and the entire abdominal wound is then covered with
polyurethane (PU) foam to seal the OA, preventing further spillage of the enteric contents. The
foam is covered with an adhesive drape and continuous negative pressure is applied. In case of large
fistulae with protruding mucosa, Tavusbay et al. suggest that the OA is covered with a perforated
polyethylene sheet, cutting a hole in the PU foam to match the fistula mouth, and the PU foam is
placed onto the polyethylene sheet.
Patients with multiple fistulae provide an even more challenging situation. Most of the
techniques described in the literature are complex and time consuming and often require a wide free
surface to properly position the diverting device. In contrast, the Baby Bottle Nipple Diversion is
quick and easy to apply, low in cost and requires very little space, thus allowing its application in
cases of multiple fistulae, whether they are far apart or in close proximity to each other.
In our experience, the Baby Bottle Nipple Diversion approach offers the best chance of
diverting the fistula output where there are multiple fistulae, either in close proximity or when
located far from each other. This allows for effective control of ongoing sepsis and promotes clean
granulation formation over the exposed bowel. It also allows exact quantification of the fistula
output and assessment of its characteristics. Table 3 provides the appropriate take home messages.
CONCLUSIONS
To the best of our knowledge, an algorithm for EAF management has never been proposed or
validated. The ever expanding variety of management techniques, as well as the increasing number
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of review papers[16,40]]
attempting to summarize them, mirror the great confusion that accompanies
the finding of an EAF and reflects the need for a rationale approach to EAF management.
The proposed flowchart in Figure 7, is derived from our surgical experience in managing the
open abdomen and EAF and from an extensive review of the available literature. Given the rarity of
this condition and the low likelihood of a controlled trial, our conclusions are not “evidence based”.
Rather, they are based on small case series and expert opinion. Because of the peculiarity of this
field, and the absolute lack of management guidelines, the opinion of expert surgeons is a major
resource in EAF treatment.
This flowchart may be an invaluable tool for those surgeons facing this surgical challenge.
Furthermore, the standardization of the approach to an EAF can lead to a better understanding of
the available literature. Speaking the same language all over the world is the first step in creating a
rational approach to EAF management and, eventually, the promulgation of internationally accepted
guidelines.
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29. Al-Khoury G, Kaufman D, Hirshberg A. Improved Control of Exposed Fistula in the Open
Abdomen. Journal of the American College of Surgeons 2008;206:397-8.
30. Layton B, DuBose J, Nichols S, et al. Pacifying the open abdomen with concomitant
intestinal fistula: a novel approach. Am J Surg 2010;199:e48-e50.
31. Rekstad LC, Wasmuth HH, Ystgaard B, et al. Topical negative-pressure therapy for small
bowel leakage in a frozen abdomen. Journal of Trauma and Acute Care Surgery
2013;75:487-91.
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32. Wang G, Ren J, Liu S, et al.. ‘‘Fistula patch’’: Making the treatment of enteroatmospheric
fistulae in the open abdomen easier. Journal of Trauma and Acute Care Surgery
2013;74:1175-7.
33. Ozer MT, Sinan H, Zeybek N, Peker Y. A simple novel technique for enteroatmospheric
fistulae: silicone fistula plug. International wound journal 2014;11 Suppl 1:22-4.
34. Sriussadaporn S, Sriussadaporn S, Kritayakirana K, Pak-art R. Operative Management of
Small Bowel Fistulae Associated with Open Abdomen. Asian Journal of Surgery 2006;29:1-
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fistulae in the open abdomen using a pedicle flap. J Surg Case Rep 2012;2012:5.
36. Al-Nahawi M. A rare approach to entero-atmospheric fistula. In: Am J Case Rep; 2013:476-
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37. Clark CE, Walker T, Bacon L, et al. Staged suspension of an enteroatmospheric fistula: a
novel surgical approach. Am Surg 2013;79:E139-40.
38. Di Saverio S, Villani S, Biscardi A, et al. Open Abdomen With Concomitant
Enteroatmospheric Fistula: Validation, Refinements, and Adjuncts to a Novel Approach.
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39. Schecter WP, HIRSHBERG A, Chang DS, et al. Enteric Fistulas: Principles of
Management. ACS 2009;209:484-91.
40. Terzi C, Egeli T, Canda AE, Arslan NC. Management of enteroatmospheric fistulae.
International wound journal 2014;11 Suppl 1:17-21.
.
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Table 1. Fistula Management Techniques
Technique Technique description PROs CONs
Estimated cost
of the
equipment
Technical
difficulty
Baby Bottle Nipple
Diversion
A baby bottle nipple is placed over the fistula with a
ring of colostomy paste. A Foley catheter is placed
inside the fistula hole and pulled through the nipple
tip. Everything is then kept in place with a
commercial NPWT dressing.
- Feasible even in
case of multiple
fistulae
- Quick and easy to
apply
- Not applicable in
case of fistulae
larger than the teat $$ Low
NPWT A simple, hand-made NPWT dressing is placed over
the open abdomen.
- Quickest and
easiest to apply
- Atraumatic
- Does not provide
effective fistula
effluent diversion
$$ Low
Baby Bottle Nipple
VAC
A baby bottle nipple is placed over the fistula with a
ring of colostomy paste. A Malecot catheter is
pulled through the nipple tip. Everything is then kept
in place with a commercial NPWT dressing.
- Feasible even in
case of multiple
fistulae
- Quick and easy to
apply
- Teat easily
displaced during
nursing maneuvers $$ Low
Floating Stoma A plastic silo placed over the open abdomen and
openings are created to fit the fistula. The edges of
these openings are sutured to the margins of the
fistula with a continuous polypropylene suture. A
stoma bag is then placed over this “floating stoma”.
- Adjustable to the
dimension of the
fistula
- Good seal
- Very traumatic
(running sutures
can lacerate bowel
wall)
$ High
Tube VAC Fistula is intubated with a Malecot catheter and the
surface of the open abdomen is covered with
petroleum-impregnated gauge. The wound is then
covered with a polyurethane sponge and the Malecot
catheters are pulled through it.
Everything is then kept in place with a commercial
NPWT dressing.
- Feasible even in
case of multiple
fistulae
- Quick and easy to
apply
- Risk of
enlargement of
fistula (there is no
stop to catheter
movements)
- Not applicable to
fistulae larger than
the catheter
$$ Low
Fistula VAC A sheet of Xeroform dressing is placed to protect
the wound bed, with a hole cut for the enteric
opening. The VAC sponge is placed over the
Xeroform layer. An adherent polyurethane drape is
eventually placed over the sponge and a hole is cut
in this drape directly over the fistula, to allow
- Quick and easy to
apply
- Atraumatic
- Risk of pooling of
enteric contents
under sponge
- Large area around
the fistula exposed
to bowel content
$$ Low
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placement of the appliance of an ostomy bag for
collecting the fistula effluent.
VAC Chimney A chimney is created with a white sponge dressing.
A plastic tube, shorter than the chimney, is then
placed into the chimney itself, to avoid its collapse.
Everything is then kept in place with a commercial
NPWT dressing, placing the connector to the pump
directly over the chimney.
- Allows
progressive
abdominal wall
closure
- Application of
aspiration directly
over the fistula
- Risk of pooling of
enteric contents
under the sponge
- Complex tand
time consuming
$$ High
Biological Dressing Human Acellular Dermal Matrix or Cadaveric Split-
thickness Skin Graft) are applied over small fistulae
or deserosalization. Fibrin glue can improve the
outcome, keeping them in place and effectively
sealing the fistula. Cyanoacrylates may be beneficial
as an adjunct to primary suturing.
- When successful
provides
immediate closure
of the fistula
- Expensive
- Not applicable if
ongoing
peritonitis/sepsis $$$ High
Primary Suture A usual suture is used to seal the fistula. Adjunct of
Cyanoacrylates and/or fibrin glue can improve
outcome.
- When successful
provides
immediate closure
of the fistula
- Quick
- Traumatic
- Risk of
enlargement of
fistula
$ Medium
Cyanoacrylates –
Fibrin Glue
Fibrin glue can improve the outcome in adjunct to
biological dressings or primary suture.
Cyanoacrylates may be beneficial as an adjunct to
primary suturing.
- When successful
provides
immediate closure
of the fistula
- Atraumatic
- Applicable as
adjunct to primary
suture or
biological
dressings
- Not applicable to
large fistulae
- Often fails to close
the fistula
$ Low
Pedicle flaps Different types of pedicle flaps are described in
literature. They should be designed and adapted
according to the specific anatomy of every single
case.
- When successful
allows quick
reconstruction of
abdominal wall
- Not applicable if
ongoing
peritonitis/sepsis
- Technically
demanding
$
Very
High
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Legend of costs ranges: $=low cost range (approximately <250 USD), $$=intermediate cost range (approx 250-1500 USD), $$$=high cost
range (approx >1500 USD)
Fistula Plug Vicryl suture is passed through the center of a
circular silicone layer and then tied to a rubber band,
with a bridge of foam-covered aluminium. The
silicone plug is then rolled and inserted into the
fistula hole and the plug is hung on the bridge.The
bridge is fixed to the abdominal wall. When the
fistula is closed, the tread is cut off and the silicon
plug is discharged at the time of defecation.
- Tight sealing of
fistula output
- Promotes fistula
closure
- Complex
- Difficult nursing
care
- Risk of bowel
obstruction
$ High
Fistula Patch Sutures are placed through the center of a gel
lamellar circle and are fixed to a drain tube placed
across the fistula outside the bowel. The gel lamellar
is then folded and pushed into the fistula, where it
will unwrap, acting like a patch inside the bowel.
The fistula patch remains in situ until the definitive
fistula takedown operation.
- Tight sealing of
fistula output
- Not tested in case
of ongoing
peritonitis, nor in
case of multiple
fistulae
- Must remain in
situ until definitive
fistula takedown
$ High
Fistula Suspension Fistula edges are gently mobilized and tacked to the
lateral aspect of the dermis. This allows the fistula to
maturate into an ostomy. Negative pressure is
applied to the granulating open abdomen.
- Artificial creation
of a fistula tract
- Allows
reconstruction of
abdominal wall
- Applicable only if
adjacent well
vascularized
dermis
- Traumatic to
fistula edges
$ High
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Table 2. EAF Classification
Anatomic location Proximal Stomach, duodenum, jejunum,
proximal ileus
Distal Distal ileus, colon
Output volume Low < 200 mL/24h
Moderate 200 – 500 mL/24h
High > 500 mL/24h
Location inside the open abdomen Superficial Drains on top of a granulating
abdominal wound
Deep Drains intestinal content inside the
peritoneal cavity
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Table 3. Take Home Messages
1. An Enteroatmospheric fistula (EAF) is a major surgical complication that offers an extremely
challenging range of critical care burdens including the full spectrum of surgical, metabolic, nutritional and
nursing issues.
2. Because spontaneous closure is extremely rare, the acute fistula management should aim to completely
divert fistula output, protect the surrounding viscera and allow the clean granulation of exposed bowel, thus
promoting the fistula to become chronic and controlled; fistula takedown and abdominal wall reconstruction
should be delayed optimally by at least 8 – 12 months.
3. Significant heterogeneity in the surgical techniques described for EAF management remains and there is
no single approach that has proven to be ideal in every circumstance: a rationale approach to EAF
management is needed.
4. The Baby Bottle Nipple Diversion approach offers the best chance of diverting the fistula output in case
of multiple fistulae, either when located in close proximity or far from each other.
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Figure Legends
Figure 1. From upper-left to lower-right, (A)(B) application of colostomy paste underlining the
nipple, (C) the complex nipple tube is held over the fistula hole with the aid of the paste layer, (D)
the NWPT drape is positioned and the nipple tube is extended through the exterior of the drape.
Figure 2. From upper-left to lower-right; (A) the fistula hole is visible over the frozen viscera, (B)
the baby nipple is cut and appropriately shaped to allow the passage of a Pezzer tube or a Foley
catheter, (C) the Foley catheter may be inserted into the fistula hole through the nipple tip and the
nipple itself is positioned around the fistula to drain the fistula leakage, (D) final result of the
exterior isolated EAF after negative pressure application over the remaining abdominal viscera.
Figure 3. Patient 2, Complete Baby Bottle Nipple Diversion dressing for multiple fistulas.
Figure 4 Patient 1, at follow up three years later, (A) frontal, (B) angled, and (C) lateral views.
Figure 5. Patient 1; three years follow-up, CT scan showing the evolution of the abdomen and the
large herniation of intra-abdominal organs. Only a thin skin layer is covering the viscera.
Figure 6. Patient 2; intraoperative appearance demonstrating good granulation over the exposed
bowel and an optimum diversion of bowel content.
Figure 7. Flowchart summarizing the various options available for EAF treatment.
Video Legends
Video 1. Patient 2, Baby Bottle Nipple Diversion technique.
Video 2. Patient 1, CT
Video 3. Patient 2, Baby Bottle Nipple Diversion technique, a strategy for multiple fistulas
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Open Abdomen EAF Management

  • 1. Accepted Manuscript Open Abdomen with Concomitant Entero-Atmospheric Fistula: Attempt to Rationalize the Approach to a Surgical Nightmare and Proposal of a Clinical Algorithm Salomone Di Saverio , MD, Antonio Tarasconi , MD., Kenji Inaba , MD, FACS, Pradeep Navsaria , MBChB, FCS(SA), FACS, Federico Coccolini , MD, David Costa Navarro , MD, Matteo Mandrioli , Panteleimon Vassiliu , MD, FACS, Elio Jovine , MD, Fausto Catena , MD, Gregorio Tugnoli , MD PII: S1072-7515(14)01845-6 DOI: 10.1016/j.jamcollsurg.2014.11.020 Reference: ACS 7650 To appear in: Journal of the American College of Surgeons Received Date: 5 September 2014 Revised Date: 8 November 2014 Accepted Date: 12 November 2014 Please cite this article as: Di Saverio S, Tarasconi A, Inaba K, Navsaria P, Coccolini F, Navarro DC, Mandrioli M, Vassiliu P, Jovine E, Catena F, Tugnoli G, Open Abdomen with Concomitant Entero-Atmospheric Fistula: Attempt to Rationalize the Approach to a Surgical Nightmare and Proposal of a Clinical Algorithm, Journal of the American College of Surgeons (2014), doi: 10.1016/ j.jamcollsurg.2014.11.020. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
  • 2. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT Open Abdomen with Concomitant Entero-Atmospheric Fistula: Attempt to Rationalize the Approach to a Surgical Nightmare and Proposal of a Clinical Algorithm Salomone Di Saverio, MD (1), Antonio Tarasconi, MD. (2), Kenji Inaba, MD, FACS (3), Pradeep Navsaria, MBChB, FCS(SA), FACS (4), Federico Coccolini, MD (5), David Costa Navarro, MD (6), Matteo Mandrioli (1), Panteleimon Vassiliu, MD, FACS (7), Elio Jovine, MD (1), Fausto Catena, MD (2), Gregorio Tugnoli, MD (1), (1) Maggiore Hospital – Bologna Local Health District, and Emergency Surgery and Trauma Surgery Unit, Maggiore Hospital Trauma Center, Bologna, Italy. (2) Department of Emergency and Trauma Surgery - Maggiore Hospital, Parma, ITALY (3) Department of Surgery. University of Southern California, Los Angeles, USA (4) Trauma Center, Groote Schuur Hospital & University of Cape Town, South Africa (5) General and Emergency and Trauma Surgery, Hospital Papa Giovanni XXIII, Bergamo, Italy (6) Department of Surgery, Alicante University General Hospital, Alicante, Spain (7) Attikon University Hospital, Department of Surgery IV, Surgery and Traumatology, Athens, Greece Disclosure Information: Nothing to disclose. Technique partially presented at the video session, 98th Clinical Congress of the American College of Surgeons, Chicago, IL, October 2012. Management Algorithm presented at the International Trauma & Emergency Surgery Week, Alicante, Spain, June 2014. Correspondence address: Salomone Di Saverio, MD Maggiore Hospital, L.go Nigrisoli 2, Bologna Italy Fax: +390516478412 email: salo75@inwind.it Brief title: Entero-Atmospheric Fistula Management
  • 3. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT Abbreviations and Acronyms AAST = American Association for the Surgery of Trauma EAF = entero-atmospheric fistula ECF = entero-cutaneous fistula IAS = intra-abdominal sepsis NPWT = negative pressure wound therapy POD = post-operative day The development of an entero-atmospheric fistula (EAF) in the midst of an open abdomen represents a surgical nightmare, with an extremely challenging critical care problem set including the full spectrum of surgical, metabolic, nutritional and nursing issues. Spontaneous closure is rare as there is no fistula tract and there is a lack of well vascularized overlying tissue. For these reasons, the acute fistula management should aim to completely divert fistula output, protect the surrounding viscera and allow for the granulation of exposed bowel. This is difficult to achieve, because of the extreme frailty of the surrounding tissues, which are chronically injured by enteric fluids, and the multiple systemic derangements of the patient, driven by severe dehydration, electrolyte and acid/base disturbances, a hypercatabolic status and ongoing sepsis. Despite the advancements in critical care and surgical management, EAF-related mortality is still upwards of 40%[1] . Significant heterogeneity in the surgical techniques described for EAF management remains and there is no single approach that has proven to be ideal in every circumstance: the aim of this study is to develop a flowchart designed to help guide the surgeons who are caring for this devastating complication, to choose the best approach on a case-by-case basis. EAF definition, etiology and management Entero-atmospheric fistula is defined as the occurrence of an enteric fistula in the middle of an open abdomen. Specific characteristics defining EAF are: the absence of a fistula tract, the lack of well-
  • 4. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT vascularized surrounding tissue and location within an open abdomen, resulting in spillage of enteric content directly into the open peritoneal cavity. Little is known about the risk factors associated with EAF development. A recent multicenter prospective observational study by Bradley, et al.[2] has attempted to determine independent predictors for the development of entero-cutaneous fistula (ECF), entero-atmospheric fistula and abdominal sepsis (IAS) in patients undergoing damage control laparotomy after trauma. Using the AAST (American Association for the Surgery of Trauma) Open Abdomen registry they identified patients who developed ECF, EAF or IAS during open abdomen management following damage control laparotomy and they compared the groups of patients with and without complications. Interestingly, their data showed that large bowel resection, large volume resuscitation and an increasing number of re-explorations were statistically significant predictors for the development of a fistula within an open abdomen after trauma. Another recent review of the available techniques for open abdomen management found a higher incidence of EAF occurring in septic OA compared to non-septic OA (12.1% versus 3.7% respectively). Furthermore, this review did not show any evidence of a relationship between use of NPWT (Negative Pressure Wound Therapy) and fistula formation[3] .For many years the application of negative pressure has been considered the primary cause of fistula formation, but further studies have demonstrated that fistula formation rate can be as low as 5%[4,5] , even with a hand-made dressing, and that in a good proportion of cases the fistula can spontaneously heal during NPWT[6] . In a recent relatively large series of EAF in patients treated with an OA for the management of abdominal sepsis, the incidence of EAF was 54.5% (18/33)[7] . In this series the rate of spontaneous closure with NPWT was 22% (4/18). The average hospital stay was 88.89 days, the median number of VAC (Vacuum Assisted Closure) applications was 22.5, and the median duration of VAC applications 43.6 days. Mortality was as high as 44.4% (8/18). Many of the principles applied to ECF management can be also considered in the management of the EAF. The latter however are often more difficult as the unprotected bowel is
  • 5. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT friable and located within a “frozen abdomen”, precluding any possible surgical manoeuvres or resection, with the added burden of peritonitis/sepsis due to the bowel content pooling directly within the exposed peritoneal cavity. Although the optimal option would be to perform a bowel resection or at least a proximal bowel diversion, this option is invariably not feasible for multiple reasons including mesenteric retraction and edema, the “frozen abdomen” and loss of domain due to retraction of the abdominal wall. As bowel resection or proximal diversion is not feasible, EAF management should aim to[8-10] : • decrease fistula effluent: the use of total parenteral nutrition, somatostatin and its analogues[11-14] as well as a proton pump inhibitor[15] can be effective in decreasing the bowel effluent; • correct any fluid and electrolyte imbalances, acid/base derangements and reversal of the hypercatabolic state (collection, quantification and characterization of bowel effluent are of key importance); • interrupt or prevent ongoing sepsis; • divert fistula output, thus allowing granulation of the exposed bowel; • if fistula closure is impossible, allow fistula to become chronic and controlled. The goal should be to control and limit the acute phase of care. Fistula takedown and abdominal wall reconstruction should be delayed optimally by at least 8 – 12 months, in order to allow loosening of the visceral adhesions, and should be performed only when the patient is well nourished and satisfactory physiological homeostasis has been achieved. Different methods for definitive fistula takedown and bowel reconstruction are currently described in the literature[16-20] . Techniques for fistula effluent diversion A wide spectrum of treatment options for effluent diversion has been described in the literature and is often used at the discretion of the attending surgeon, as a universally accepted management
  • 6. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT algorithm does not exist. The following techniques can be individualized to patients depending on their particular characteristics. 1. Negative Pressure Wound Therapy (NPWT)– The use of negative pressure in the open abdomen with hand-made dressings is well described and some authors extended this technique to cases of EAF. This method is the easiest to apply and represents the foundation for many of the subsequent techniques. 2. Biological dressing / Fibrin Glue or Cyanoacrylates / Primary Suture[21,22] –The application of biological dressings (ie, Human Acellular Dermal Matrix or Cadaveric Split-thickness Skin Graft) has been described with good results, particularly in case of a small size fistula or deserosalization. Fibrin glue can improve the outcome of biological dressings, helping to keep them in place and effectively sealing the fistula. Cyanoacrylates may be beneficial for small EAFs, especially as an adjunct to primary suturing.[23] 3. Floating Stoma[24] –This is made with a plastic silo placed over the open abdomen, where openings are created to best fit the fistula opening; the edge of these openings are then sutured to the margins of the opening in the enteric loops with a continuous polypropylene suture. A stoma bag is then placed over this “floating stoma” in order to collect the enteric effluent. 4. Fistula VAC[25] –This method is easy and quick to apply, consisting of a single sheet of Xeroform dressing placed to protect the wound bed, with a hole cut for the enteric opening. The VAC sponge is accurately tailored to fit the wound and to match the fistula opening, and is placed over the Xeroform layer. An adherent polyurethane drape is eventually placed over the sponge and a hole is cut in this drape directly over the fistula, to allow placement of the appliance of an ostomy bag for collecting the fistula effluent. A number of refinements to this technique are described in literature, all attempting to obtain a better sealing of fistula area from the rest of the wound[26-28] .
  • 7. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT 5. Tube VAC[29] –The EAF is intubated with Malecot catheters and the surface of the open abdomen is covered with petroleum-impregnated gauge. The wound is then covered with a polyurethane sponge and the Malecot catheters are pulled through it. The entire device is then sealed with an occlusive dressing and a continuous negative pressure is applied. 6. Baby Bottle Nipple VAC[30-38] –A baby bottle rubber nipple is placed over the fistula opening and a Pezzer tube, Malecot or Foley catheter is placed through a small hole cut into the tip of the nipple. A round layer of colostomy paste can be placed under the nipple in order to ensure a better seal. A petroleum jelly-impregnated gauge or clear Telfa sheet is then placed over the bowel and the entire wound is covered by a commercial VAC dressing. A small hole is shaped into the VAC sponge, to hold the nipple in place. 7. VAC Chimney[31] – A chimney is created with a white sponge dressing, with the base of this construct covering the adjacent healthy tissue for an area of 2-3 cm, to avoid leakage of bowel effluent. A plastic tube, shorter than the chimney, is then placed into the chimney itself, to avoid its collapse. The open abdomen is then covered with a conventional VAC dressing, placing the connector to the pump directly over the chimney. 8. Fistula Patch[32] – A soft, flexible gel lamellar is shaped into a round form. Sutures are then placed through the center of this circle and fixed to a drain tube placed across the fistula, outside of the bowel. The silica gel lamellar is then folded and pushed into the fistula. Once inside the bowel it will unwrap, acting like a patch inside the bowel. The fistula patch would then remain in situ until the definitive fistula takedown operation. Some authors have recently described a similar technique using a patch of hydrophilic polyvinyl alcohol foam to cover small fistulas, combined with NPWT used on the remaining abdominal surface4 . 9. Fistula Plug[33] – Thisisa plug designed to seal the EAF from inside consisting ofa circular disk of 1mm thick silicone with a diameter of 2-5 cm. A Vicryl suture is passed through the center of the silicon circle and then tied to a rubber band, with a bridge of foam-covered aluminium. The silicone plug is then rolled and inserted into the fistula hole, the plug is
  • 8. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT hung on the bridge by means of the suspension suture and rubber band. The bridge is fixed to the abdominal wall using a self-adhesive plaster. Eventually, when the fistula is closed, the tread will be cut off and the silicon plug will be discharged at the time of defecation. 10. Pedicled flap– Different types of flaps have been described in the literature[18,34-36] . Although feasible and possibly effective, they are highly technically demanding and require a well- stabilized patient, without ongoing sepsis or physiological derangements. For these reasons, flaps remain a good option for definitive management, after the acute phase has resolved. 11. Suspension / Stoma Conversion[36,37] – In selected cases, when the fistula is located near to the edge of the abdominal wound, the fistula edges can be gently mobilized and tacked to the lateral aspect of the dermis. This allows the fistula to maturate into a definitive ostomy, while negative pressure is applied to the granulating open abdomen, which is now protected from bowel effluent. The pros and cons, estimated cost and technical difficulty of every approach are summarized in Table 1. Costs have been estimated, because the prices of every device and surgical item vary widely between different countries and hospitals. A NPWT device rental price of 997,50 € was utilized for the estimates. Baby Bottle Nipple Diversion – Description of the technique We have developed a refinement[38] of the technique previously described by Layton[30] et al., improving what we have found to be the practical downsides of this interesting management option for an EAF. This has been named the baby bottle nipple diversion. First, the fistula is exteriorized as much as possible outside the abdominal cavity, thus creating a flat surface that will allow optimal nipple placement. At this time, irrigation and exploration of the abdominal cavity should be performed, to reduce peritoneal contamination and decrease ongoing sepsis. After these preliminary steps, a baby bottle nipple of soft silicone is placed over the fistula (Video 1). The tip of the nipple is cut and a small size Pezzer tube is pulled through the hole of the
  • 9. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT rubber nipple and secured in place by non-absorbable stitch tied around the tip of the nipple (Video 1). In order to achieve a better seal, an underlying layer of colostomy paste (Figure 1) can be placed around the fistula and under the nipple, which is then surrounded by a jelly gauze, covering the bowel and excluding the area of the fistula. We have modified Layton’s technique to further optimize the external diversion of the fistula and minimize nipple dislocation by inserting a small (10 Fr) Foley catheter (Figure 2) into the fistula opening and inflating the balloon gently with 2 to 3 cc of water. The Foley catheter is then passed through and secured to the silicone nipple neck. Finally a NPWT dressing system is placed over the exposed viscera to promote surface granulation (Video 1: Renasys™, Smith & Nephew Corporate). The plastic drape is placed over the open abdomen and the nipple–tube complex is passed through a hole shaped within the drape and the sponge. The plastic drape is then used to cover the sponge and shaped around the Pezzer tube. The negative pressure is used to compress the dressing, hold the nipple in place and sealoff the fistula (see Figure 3) The baby bottle nipple diversion has the advantage of being effective even in cases of large, high output fistulae and, unlike other techniques, can also be effective in case of multiple fistulae. Clinical validation, patient 1 In October 2010 we applied this novel approach to the case of a 46-yearold male admitted for complete adhesive small bowel obstruction and strangulation of a parastomal hernia, who developed on postoperative day 7 two ileal perforations within a completely frozen abdomen. These were initially treated with fibrin glue and an open abdomen with BogotĂĄ Bag. After 6 days of NPWT therapy, a leak from one of the previously repaired perforations appeared. A further attempt at direct repair with Vicryl stitches and fibrin glue was not successful and the baby bottle nipple diversion was utilized. After three months of treatment with NPWT and baby bottle nipple diversion, the fistula output was diverted, effectively functioning as an ileostomy. The abdominal surface was almost
  • 10. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT completely covered by skin and subcutaneous tissue granulating from the edges of the abdominal wall (Video 2 – CT scan); the patient was therefore discharged to a rehabilitation facility. After three year follow-up, (Figure 4a, Figure 4b, Figure 4c) the patient has returned to a normal active life with good quality of life. The previous EAF is functioning well as a natural ileostomy. The open abdomen has evolved into a large herniation of intra-abdominal organs and only a thin skin layer is covering the viscera (Figure 5 – three years follow-up CT scan). Clinical validation, patient 2 In June 2013 we had to face a similar surgical nightmare: a 73-yearold male was admitted for acute bleeding from multiple angiodysplastic foci and underwent emergent right colonic resection. On POD #7 the hospital course was complicated by evisceration and ileal non-anastomotic perforation. This was treated with ileal resection and primary anastomosis. Later on, the patient underwent two subsequent re-laparotomies for evisceration and small bowel perforations. This was further complicated by a massive abdominal wall necrotizing fascitis, which caused a great loss of tissue within the abdominal wall and required NPWT dressing. After 32 days and 14 NPWT dressing changes, two ileal EAF appeared within a few centimeters from each other. At this point the abdomen was frozen and completely inaccessible, due to heavy matted adhesions. Based on the satisfactory results of our previous experience, the Baby bottle nipple diversion technique was utilized, even in the presence of these multiple fistulas (Video 3). Two separate baby bottle nipples were placed over the fistulae, allowing effective and separate isolation of the two different EAFs (Figure 3). After four dressing changes, both fistulae were well controlled and both their size and output had strongly decreased. The surrounding viscera were covered with Renasys™ dressing, (Smith & Nephew Corporate) and treated with low pressure (-60 to -80 mmHg) NPWT. In the absence of significant enteric contamination, a clean granulation bed was formed.
  • 11. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT On POD #65, the patient died of acute pulmonary edema, secondary to myocardial infarction. At this stage, the fistulae were well controlled and the abdomen was clean and rapidly granulating (Figure 6). Our proposal The management of an EAF is extremely challenging and should be tailored to the specific characteristics of each case. We believe that a systematic approach to the management of this devastating problem is required. Therefore, after performing a comprehensive review of the literature and analyzing the different options for EAF management, we have developed a flowchart, merging all the techniques described to date and including our experience and techniques (Figure 7). This is one rational, practical method for approaching this surgical challenge. The acute management of an EAF should aim to: 1) divert the fistula output, thus preventing the spreading of intestinal fluid into the peritoneal cavity; 2) collect and quantify the fistula output, in order to address and correct fluids and electrolyte imbalances; 3) protect and keep clean the surrounding granulating viscera. A thorough classification of EAF is essential for choosing the correct approach. According to the literature, an EAF can be classified based on anatomic location (proximal/distal); fistula output volume (low/moderate/high) and location in the open abdomen (superficial/deep) [10,16,39] (Table 2). It is well known that distal and low-output fistulas have a higher spontaneous closure rate than those that are more proximal and with high-output. For this reason, in the case of de-serozalisation and distal, small or low output fistulas, a first attempt at primary closure with sutures and sealants (fibrin glue, cyanoacrylates)[21,23] should be made. If this first attempt fails, the fistula must be approached in the same manner as a proximal, large or moderate/high output fistulae. The latter fistulae type is very unlikely to close with a glue/suture approach. The presence of ongoing peritonitis should be the factor that drives the choice of the management technique. Biologic dressings and flaps or skin grafting should be avoided in these cases with ongoing
  • 12. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT uncontrolled peritonitis, because of the high probability of failure (ie, graft rejection, flap necrosis and lack of sepsis control). If there is ongoing peritonitis, the primary aim of treatment should be the diversion of fistula output, allowing improvement of the physiological condition of the patient. In the most recent review on the management of EAF4 , Tavusbay et al. proposed different techniques according to the size/output of the fistula. Small fistulae are first covered with a patch of hydrophilic polyvinyl alcohol foam and the entire abdominal wound is then covered with polyurethane (PU) foam to seal the OA, preventing further spillage of the enteric contents. The foam is covered with an adhesive drape and continuous negative pressure is applied. In case of large fistulae with protruding mucosa, Tavusbay et al. suggest that the OA is covered with a perforated polyethylene sheet, cutting a hole in the PU foam to match the fistula mouth, and the PU foam is placed onto the polyethylene sheet. Patients with multiple fistulae provide an even more challenging situation. Most of the techniques described in the literature are complex and time consuming and often require a wide free surface to properly position the diverting device. In contrast, the Baby Bottle Nipple Diversion is quick and easy to apply, low in cost and requires very little space, thus allowing its application in cases of multiple fistulae, whether they are far apart or in close proximity to each other. In our experience, the Baby Bottle Nipple Diversion approach offers the best chance of diverting the fistula output where there are multiple fistulae, either in close proximity or when located far from each other. This allows for effective control of ongoing sepsis and promotes clean granulation formation over the exposed bowel. It also allows exact quantification of the fistula output and assessment of its characteristics. Table 3 provides the appropriate take home messages. CONCLUSIONS To the best of our knowledge, an algorithm for EAF management has never been proposed or validated. The ever expanding variety of management techniques, as well as the increasing number
  • 13. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT of review papers[16,40]] attempting to summarize them, mirror the great confusion that accompanies the finding of an EAF and reflects the need for a rationale approach to EAF management. The proposed flowchart in Figure 7, is derived from our surgical experience in managing the open abdomen and EAF and from an extensive review of the available literature. Given the rarity of this condition and the low likelihood of a controlled trial, our conclusions are not “evidence based”. Rather, they are based on small case series and expert opinion. Because of the peculiarity of this field, and the absolute lack of management guidelines, the opinion of expert surgeons is a major resource in EAF treatment. This flowchart may be an invaluable tool for those surgeons facing this surgical challenge. Furthermore, the standardization of the approach to an EAF can lead to a better understanding of the available literature. Speaking the same language all over the world is the first step in creating a rational approach to EAF management and, eventually, the promulgation of internationally accepted guidelines.
  • 14. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT REFERENCES 1. Becker HP, Willms A, Schwab R. Small bowel fistulas and the open abdomen. Scand J Surg 2007;96:263-71. 2. Bradley MJ, Dubose JJ, Scalea TM, et al. Independent predictors of enteric fistula and abdominal sepsis after damage control laparotomy: results from the prospective AAST Open Abdomen registry. JAMA surgery 2013;148:947-54. 3. Bruhin A, Ferreira F, Chariker M, et al. Systematic review and evidence based recommendations for the use of Negative Pressure Wound Therapy in the open abdomen. Int J Surg 2014;12:1105-14. 4. Navsaria P, Nicol A, Hudson D, et al. Negative pressure wound therapy management of the "open abdomen" following trauma: a prospective study and systematic review. World J Emerg Surg 2013;8:4. 5. Navsaria PH, Bunting M, Omoshoro-Jones J, et al. Temporary closure of open abdominal wounds by the modified sandwich-vacuum pack technique. Br J Surg 2003;90:718-22. 6. Kirshtein B, Mizrahi S. Vacuum-assisted management of enteroatmospheric fistula within the open abdomen. Am Surg 2014;80:209-10. 7. Tavusbay C, Genc H, Cin N, et al. Use of a vacuum-assisted closure system for the management of enteroatmospheric fistulae. Surg Today 2014. 8. Schecter WP. Management of Enterocutaneous Fistulas. Surg Clin North Am 2011;91:481- 91. 9. Davis KG, Johnson EK. Controversies in the Care of the Enterocutaneous Fistula. Surg Clin North Am 2013;93:231-50. 10. Evenson A, Fischer J. Current Management of Enterocutaneous Fistula. Journal of gastrointestinal surgery : official journal of the Society for Surgery of the Alimentary Tract 2006;10:455-64.
  • 15. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT 11. Coughlin S, Roth L, Lurati G, Faulhaber M. Somatostatin analogues for the treatment of enterocutaneous fistulas: a systematic review and meta-analysis. World J Surg 2012;36:1016-29. 12. Stevens P, Foulkes RE, Hartford-Beynon JS, Delicata RJ. Systematic review and meta- analysis of the role of somatostatin and its analogues in the treatment of enterocutaneous fistula. European journal of gastroenterology & hepatology 2011;23:912-22. 13. Rahbour G, Siddiqui MR, Ullah MR, et al. A meta-analysis of outcomes following use of somatostatin and its analogues for the management of enterocutaneous fistulas. Ann Surg 2012;256:946-54. 14. Lloyd DA, Gabe SM, Windsor AC. Nutrition and management of enterocutaneous fistula. Br J Surg 2006;93:1045-55. 15. Nightingale JM. The medical management of intestinal failure: methods to reduce the severity. The Proceedings of the Nutrition Society 2003;62:703-10. 16. Marinis A, Gkiokas G, Argyra E, et al. "Enteroatmospheric fistulae" - gastrointestinal openings in the open abdomen: a review and recent proposal of a surgical technique. Scand J Surg 2013;102:61-8. 17. Krpata DM, Stein SL, Eston M, et al. Outcomes of simultaneous large complex abdominal wall reconstruction and enterocutaneous fistula takedown. AJS 2013;205:354-9. 18. Wind J, van Koperen PJ, Slors JFM, Bemelman WA. Single-stage closure of enterocutaneous fistula and stomas in the presence of large abdominal wall defects using the components separation technique. AJS 2009;197:24-9. 19. Dionigi G, Dionigi R, Rovera F, et al. Treatment of high output entero-cutaneous fistulae associated with large abdominal wall defects: Single center experience. International Journal of Surgery 2008;6:51-6. 20. Demetriades D. A Technique of Surgical Closure of Complex Intestinal Fistulae in the Open Abdomen. The Journal of Trauma: Injury, Infection, and Critical Care 2003;55:999-1001.
  • 16. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT 21. Girard S, Sideman M, Spain DA. A novel approach to the problem of intestinal fistulization arising in patients managed with open peritoneal cavities. AJS 2002;184:166-7. 22. Jamshidi R, Schecter WP. Biological dressings for the management of enteric fistulas in the open abdomen: a preliminary report. Arch Surg 2007;142:793-6. 23. Bhat YM, Banerjee S, Barth BA, et al. Tissue adhesives: cyanoacrylate glue and fibrin sealant. Gastrointestinal Endoscopy 2013;78:209-15. 24. Subramaniam MH, Liscum KR, Hirshberg A. The floating stoma: a new technique for controlling exposed fistulae in abdominal trauma. The Journal of Trauma: Injury, Infection, and Critical Care 2002;53:386-8. 25. Goverman J, Yelon JA, Platz JJ, et al. The "Fistula VAC," a Technique for Management of Enterocutaneous Fistulae Arising within the Open Abdomen: Report of 5 Cases. The Journal of Trauma: Injury, Infection, and Critical Care 2006;60:428-31. 26. D'Hondt M, Devriendt D, Van Rooy F, et al. Treatment of small-bowel fistulae in the open abdomen with topical negative-pressure therapy. AJS 2011;202:e20-e4. 27. Piazza R, Armstrong S, Vanderkolk W, et al. A Modified “Fistula-VAC” Technique: Management of Multiple Enterocutaneous Fistulas in the Open Abdomen. Plastic and Reconstructive Surgery 2009;124:453e-5e. 28. Pang TC, Morton J, Pincott S. Novel technique for isolating and dressing enteroatmospheric fistulae. ANZ J Surg 2012;82:747-9. 29. Al-Khoury G, Kaufman D, Hirshberg A. Improved Control of Exposed Fistula in the Open Abdomen. Journal of the American College of Surgeons 2008;206:397-8. 30. Layton B, DuBose J, Nichols S, et al. Pacifying the open abdomen with concomitant intestinal fistula: a novel approach. Am J Surg 2010;199:e48-e50. 31. Rekstad LC, Wasmuth HH, Ystgaard B, et al. Topical negative-pressure therapy for small bowel leakage in a frozen abdomen. Journal of Trauma and Acute Care Surgery 2013;75:487-91.
  • 17. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT 32. Wang G, Ren J, Liu S, et al.. ‘‘Fistula patch’’: Making the treatment of enteroatmospheric fistulae in the open abdomen easier. Journal of Trauma and Acute Care Surgery 2013;74:1175-7. 33. Ozer MT, Sinan H, Zeybek N, Peker Y. A simple novel technique for enteroatmospheric fistulae: silicone fistula plug. International wound journal 2014;11 Suppl 1:22-4. 34. Sriussadaporn S, Sriussadaporn S, Kritayakirana K, Pak-art R. Operative Management of Small Bowel Fistulae Associated with Open Abdomen. Asian Journal of Surgery 2006;29:1- 7. 35. Stephensen B, Brown J, Lambrianides A. A novel method for managing enterocutaneous fistulae in the open abdomen using a pedicle flap. J Surg Case Rep 2012;2012:5. 36. Al-Nahawi M. A rare approach to entero-atmospheric fistula. In: Am J Case Rep; 2013:476- 80. 37. Clark CE, Walker T, Bacon L, et al. Staged suspension of an enteroatmospheric fistula: a novel surgical approach. Am Surg 2013;79:E139-40. 38. Di Saverio S, Villani S, Biscardi A, et al. Open Abdomen With Concomitant Enteroatmospheric Fistula: Validation, Refinements, and Adjuncts to a Novel Approach. The Journal of Trauma: Injury, Infection, and Critical Care 2011;71:760-2. 39. Schecter WP, HIRSHBERG A, Chang DS, et al. Enteric Fistulas: Principles of Management. ACS 2009;209:484-91. 40. Terzi C, Egeli T, Canda AE, Arslan NC. Management of enteroatmospheric fistulae. International wound journal 2014;11 Suppl 1:17-21. .
  • 18. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT Table 1. Fistula Management Techniques Technique Technique description PROs CONs Estimated cost of the equipment Technical difficulty Baby Bottle Nipple Diversion A baby bottle nipple is placed over the fistula with a ring of colostomy paste. A Foley catheter is placed inside the fistula hole and pulled through the nipple tip. Everything is then kept in place with a commercial NPWT dressing. - Feasible even in case of multiple fistulae - Quick and easy to apply - Not applicable in case of fistulae larger than the teat $$ Low NPWT A simple, hand-made NPWT dressing is placed over the open abdomen. - Quickest and easiest to apply - Atraumatic - Does not provide effective fistula effluent diversion $$ Low Baby Bottle Nipple VAC A baby bottle nipple is placed over the fistula with a ring of colostomy paste. A Malecot catheter is pulled through the nipple tip. Everything is then kept in place with a commercial NPWT dressing. - Feasible even in case of multiple fistulae - Quick and easy to apply - Teat easily displaced during nursing maneuvers $$ Low Floating Stoma A plastic silo placed over the open abdomen and openings are created to fit the fistula. The edges of these openings are sutured to the margins of the fistula with a continuous polypropylene suture. A stoma bag is then placed over this “floating stoma”. - Adjustable to the dimension of the fistula - Good seal - Very traumatic (running sutures can lacerate bowel wall) $ High Tube VAC Fistula is intubated with a Malecot catheter and the surface of the open abdomen is covered with petroleum-impregnated gauge. The wound is then covered with a polyurethane sponge and the Malecot catheters are pulled through it. Everything is then kept in place with a commercial NPWT dressing. - Feasible even in case of multiple fistulae - Quick and easy to apply - Risk of enlargement of fistula (there is no stop to catheter movements) - Not applicable to fistulae larger than the catheter $$ Low Fistula VAC A sheet of Xeroform dressing is placed to protect the wound bed, with a hole cut for the enteric opening. The VAC sponge is placed over the Xeroform layer. An adherent polyurethane drape is eventually placed over the sponge and a hole is cut in this drape directly over the fistula, to allow - Quick and easy to apply - Atraumatic - Risk of pooling of enteric contents under sponge - Large area around the fistula exposed to bowel content $$ Low
  • 19. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT placement of the appliance of an ostomy bag for collecting the fistula effluent. VAC Chimney A chimney is created with a white sponge dressing. A plastic tube, shorter than the chimney, is then placed into the chimney itself, to avoid its collapse. Everything is then kept in place with a commercial NPWT dressing, placing the connector to the pump directly over the chimney. - Allows progressive abdominal wall closure - Application of aspiration directly over the fistula - Risk of pooling of enteric contents under the sponge - Complex tand time consuming $$ High Biological Dressing Human Acellular Dermal Matrix or Cadaveric Split- thickness Skin Graft) are applied over small fistulae or deserosalization. Fibrin glue can improve the outcome, keeping them in place and effectively sealing the fistula. Cyanoacrylates may be beneficial as an adjunct to primary suturing. - When successful provides immediate closure of the fistula - Expensive - Not applicable if ongoing peritonitis/sepsis $$$ High Primary Suture A usual suture is used to seal the fistula. Adjunct of Cyanoacrylates and/or fibrin glue can improve outcome. - When successful provides immediate closure of the fistula - Quick - Traumatic - Risk of enlargement of fistula $ Medium Cyanoacrylates – Fibrin Glue Fibrin glue can improve the outcome in adjunct to biological dressings or primary suture. Cyanoacrylates may be beneficial as an adjunct to primary suturing. - When successful provides immediate closure of the fistula - Atraumatic - Applicable as adjunct to primary suture or biological dressings - Not applicable to large fistulae - Often fails to close the fistula $ Low Pedicle flaps Different types of pedicle flaps are described in literature. They should be designed and adapted according to the specific anatomy of every single case. - When successful allows quick reconstruction of abdominal wall - Not applicable if ongoing peritonitis/sepsis - Technically demanding $ Very High
  • 20. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT Legend of costs ranges: $=low cost range (approximately <250 USD), $$=intermediate cost range (approx 250-1500 USD), $$$=high cost range (approx >1500 USD) Fistula Plug Vicryl suture is passed through the center of a circular silicone layer and then tied to a rubber band, with a bridge of foam-covered aluminium. The silicone plug is then rolled and inserted into the fistula hole and the plug is hung on the bridge.The bridge is fixed to the abdominal wall. When the fistula is closed, the tread is cut off and the silicon plug is discharged at the time of defecation. - Tight sealing of fistula output - Promotes fistula closure - Complex - Difficult nursing care - Risk of bowel obstruction $ High Fistula Patch Sutures are placed through the center of a gel lamellar circle and are fixed to a drain tube placed across the fistula outside the bowel. The gel lamellar is then folded and pushed into the fistula, where it will unwrap, acting like a patch inside the bowel. The fistula patch remains in situ until the definitive fistula takedown operation. - Tight sealing of fistula output - Not tested in case of ongoing peritonitis, nor in case of multiple fistulae - Must remain in situ until definitive fistula takedown $ High Fistula Suspension Fistula edges are gently mobilized and tacked to the lateral aspect of the dermis. This allows the fistula to maturate into an ostomy. Negative pressure is applied to the granulating open abdomen. - Artificial creation of a fistula tract - Allows reconstruction of abdominal wall - Applicable only if adjacent well vascularized dermis - Traumatic to fistula edges $ High
  • 21. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT Table 2. EAF Classification Anatomic location Proximal Stomach, duodenum, jejunum, proximal ileus Distal Distal ileus, colon Output volume Low < 200 mL/24h Moderate 200 – 500 mL/24h High > 500 mL/24h Location inside the open abdomen Superficial Drains on top of a granulating abdominal wound Deep Drains intestinal content inside the peritoneal cavity
  • 22. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT Table 3. Take Home Messages 1. An Enteroatmospheric fistula (EAF) is a major surgical complication that offers an extremely challenging range of critical care burdens including the full spectrum of surgical, metabolic, nutritional and nursing issues. 2. Because spontaneous closure is extremely rare, the acute fistula management should aim to completely divert fistula output, protect the surrounding viscera and allow the clean granulation of exposed bowel, thus promoting the fistula to become chronic and controlled; fistula takedown and abdominal wall reconstruction should be delayed optimally by at least 8 – 12 months. 3. Significant heterogeneity in the surgical techniques described for EAF management remains and there is no single approach that has proven to be ideal in every circumstance: a rationale approach to EAF management is needed. 4. The Baby Bottle Nipple Diversion approach offers the best chance of diverting the fistula output in case of multiple fistulae, either when located in close proximity or far from each other.
  • 23. M ANUSCRIPT ACCEPTED ACCEPTED MANUSCRIPT Figure Legends Figure 1. From upper-left to lower-right, (A)(B) application of colostomy paste underlining the nipple, (C) the complex nipple tube is held over the fistula hole with the aid of the paste layer, (D) the NWPT drape is positioned and the nipple tube is extended through the exterior of the drape. Figure 2. From upper-left to lower-right; (A) the fistula hole is visible over the frozen viscera, (B) the baby nipple is cut and appropriately shaped to allow the passage of a Pezzer tube or a Foley catheter, (C) the Foley catheter may be inserted into the fistula hole through the nipple tip and the nipple itself is positioned around the fistula to drain the fistula leakage, (D) final result of the exterior isolated EAF after negative pressure application over the remaining abdominal viscera. Figure 3. Patient 2, Complete Baby Bottle Nipple Diversion dressing for multiple fistulas. Figure 4 Patient 1, at follow up three years later, (A) frontal, (B) angled, and (C) lateral views. Figure 5. Patient 1; three years follow-up, CT scan showing the evolution of the abdomen and the large herniation of intra-abdominal organs. Only a thin skin layer is covering the viscera. Figure 6. Patient 2; intraoperative appearance demonstrating good granulation over the exposed bowel and an optimum diversion of bowel content. Figure 7. Flowchart summarizing the various options available for EAF treatment. Video Legends Video 1. Patient 2, Baby Bottle Nipple Diversion technique. Video 2. Patient 1, CT Video 3. Patient 2, Baby Bottle Nipple Diversion technique, a strategy for multiple fistulas