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Enteroatmospheric fistula (EAF) is a feared and challenging complication for both the patient and care team. EAF is a subset form of enterocutaneous fistula (ECF) and characterized by the absence of the soft tissue overlying the bowel. The open abdomen (OA) is the leading cause of EAF with a high risk of fistula formation during dressing changes. The multidisciplinary approach is the key successful management. The principles EAF treatment is based on the correction of intravascular fluid deficit to reverse catabolic state, control of deep abdominal infection using image-guided drainage, control of fistula effluent, protection of the skin and the surrounding granulating tissue by using negative pressure wound therapy (NPWT) and achieving a good nutritional condition by providing PN and enteral nutrition if possible. The spontaneous closure of EAF is extremely rare and definitive reconstructive surgery is almost required. Prevention is the best way to reduce the risks of EAF to occur. This review article discusses diagnosis, etiology, management aspects and prevention of EAF with specific attention dedicated to effluent control, wound care, nutrition and definitive fistula surgery and abdominal wall reconstruction.
Keywords: Enterocutaneous fistula, Enteroatmospheric fistula, Open abdomen, Effluent control, Wound care, Nutrition-Definitive fistula surgery, Abdominal wall reconstruction
An enterocutaneous fistula (ECF) is defined as an abnormal communication between the intra-abdominal GI tract and skin and is traditionally considered as one of the most feared complications in gastrointestinal surgery. The mortality of ECF largely varied from 5% to 20% and this variation was due to the heterogeneity of the published studies [1,2]. The associated morbidity is excessive with prolonged hospital stay particularly intensive care unit stay, increased hospital cost and negative important psychological impact on the patient health . The entroatmospheric fistula (EAF) is a subset form of ECF with several unique characteristics that merit to be highlighted. Oppositely to many postoperative complications, the diagnosis of EAF is often obvious. The typical predisposing situation is the management of the open abdomen for at least several days or months. The bowel is exposed directly to the environment and dressing is made to cover the exposed bowel, keep it moist and avoid visceral trauma (Figure 1). The dressing is changed regularly and so a small erosion of exposed and fragilized bowel can occur leading to the fistula formation with drainage of intestinal content into the wound. When occurred, any closure attempt of EAF by performing simple intestinal suture is highly avoided and may result in larger bowel wall opening with aggravating management difficulties. The EAF management scheme is similar to that used in ECF and is based on a few sound tenets including recognition, stabilization, anatomic definition and definitive surgery if needed [4,5]. However major differences are the difficulty in controlling fistula effluent, skin protection, potential prevention and the complexity of abdominal wall reconstructive surgery. I importantly, a well-organized multidisciplinary approach and evaluation of these patients in a specialized centre dealing with ECFs are the keys to successful management with improved outcomes. This review article discusses diagnosis, etiology, management aspects and prevention of EAF with specific attention dedicated to effluent control, wound care, nutrition and definitive fistula surgery and abdominal wall reconstruction. INCIDENCE AND CLASSIFICATION
The reported overall incidence of EAF varied from 5%-19% [6-9] in damage control laparotomy. This variation in reported incidence was due to the indication for damage control laparotomy (trauma vs. non-trauma), the number of re-operations for abdominal procedures and the time to definitive closure. The increase in incidence was linked to the wide use of damage control laparotomy in the surgical community. Depending on location within the abdomen cavity, the enteroatmospheric fistulas are two types, deep and superficial. Deep EAFs drain directly into the abdominal cavity and so is more likely a cause of peritonitis. Superficial EAFs are completely extra peritoneal realizing a primary stoma by draining on the top or the side of the granulating abdominal wound. As the same as ECF, EAF can be classified on the basis of an involved segment of GI tract (i.e., enteroatmospheric, coloatmospheric gastro atmospheric, etc.) and on the daily output as low-output <200 mL, high output >500 mL and moderate from 200 to 500 ml.
EAF develops more commonly following an open abdomen surgery performed for trauma, after damage control and decompressive laparotomies, and in the setting of elective surgery. However, Trauma is largely the leading cause of EAF. EAF also can occur in patients who received surgery for abdominal septic process resulting in the open abdomen secondary to difficulties to achieve abdominal wall closure due to bowel edema or large fascial dehiscence’s. The physical characteristics of an open abdomen predispose to the development of EAF. Usually, the bowel is directly exposed to the environment, requiring repeated complicated abdominal dressing changes and so this condition is more likely favorable to EAF development. Despite the utmost care taken to prevent trauma during dressing changes, the multiples manipulations can be traumatic to already edematous and friable bowel resulting in bowel wall erosion and fistula formation. Moreover, the etiologies of postoperative EAF are often related to the condition that necessitated surgeries including malignancy, inflammatory intestinal diseases, adhesiolysis, abdominal sepsis, anastomotic leaks, bowel ischemia and obstruction and emergency abdominal procedures [10,11].
Clearly, prevention is the best way to reduce the risk of EAF. Therefore take precautions and preventive measures at the first laparotomy are highly recommended to prevent EAF in high-risk patient. Before closing the abdominal cavity, the greater momentum should be placed in order to cover the bowel if at all possible, and when non-absorbable mesh is used, it should never be in direct contact with bowel. The use of any temporary closure device should protect the underlying bowel and allowing access to the peritoneal cavity. As reported, damage control laparotomies were associated with a high rate of EAF if the abdomen was left open for more than 8 days [8,12]. Therefore every effort should be made to achieve closure of the open abdomen as soon as possible to decrease the EAF risk. However, it is difficult for the surgeon to determine the timing of abdomen closure. Typically, the fascia closure should be achieved without leading to intra-abdominal hypertension after the resolution of visceral edema. Several methods have been reported to reduce time to closure including Covering the viscera with a non-adherent drape and achieving skin – only closure when fascial reapproximation is not feasible, however, repetitive skin trauma may occur if multiple reoperations are needed prior to definitive closure . The planned ventral hernia (PVH) approach consists of covering the bowel with an absorbable polyglactin mesh fixed to the fascia edges. If enough available, the skin can be closed over drains placed between absorbable material and skin. Therefore the peritoneal cavity is closed with guaranteed future ventral hernia. This method became less favorable after the availability of NPWT, biologic meshes, and other early fascial closure techniques. The use of NPWT systems to achieve closure of an open abdomen has shown superior results compared to absorbable mesh [13-16] with statically no significant slightly higher rate of fistula formation (21% vs. 5%) .
When early closure is impractical after several days, the use of biologic mesh bridges to achieve fascial closure with skin reapproximation over drains or NPWT placed over the top of biologic material seems to be an attractive indication. This method achieves the goal of closure over viscera option with a lower rate of bowel fistulization . However, it is associated with a high rate of incisional hernia formation [19,20]. The progressive retraction of the rectus and oblique muscle laterally in the open abdomen can plague any effort made to achieve early closure. Therefore many techniques to prevent abdominal wall retraction have been described and some have been shown to facilitate the achievement of early abdominal wall closure [21-25]. The use of mesh material fixed to the fascial edges associated with progressive tightening at the midline as visceral edema resolves is common in all these methods. A non-adherent layer or sheet is placed over the viscera inside the peritoneal cavity to prevent adhesions to the anterior abdominal wall that potentially results in the frozen abdomen. The NPWT device is applied over the top of the mesh bridge to control fluids and exudate.
The dressing of an open abdomen should be constructed by experienced surgical team members avoiding to place gauze or negative pressure devices directly on the exposed bowel . The presence of an experienced member of the surgical team during the dressing changes of an open abdomen is imperative to unsure avoidance of underlying viscera trauma and to early recognize areas of deserolization which are likely precursors of an EAF. Finally, the surgical team should always have in mind the greater risk of fistula formation when attempting to achieve a definitive fascial closure of an open abdomen [8,9,27]. As previously stated, nutritional optimization is central in the treatment and prevention of Efate open abdomen is a source of extreme catabolic state and increased nutritional requirements. It is well demonstrated that enteral nutrition is more benefit than parenteral nutrition in surgical patients. The early enteral nutrition (less than or equal to 4 days after surgery) has been associated with a significant reduction of EAF rate and time to abdomen closure .
The management of EAF involves a lengthy and labor-intensive process broken down into phases of treatment so-called step-by-step approach [5,26]. This management scheme is similar to that used in case of ECF and is based on diagnosis and stabilization, anatomic definition and fistula reconstructive surgery if needed. Therefore, the management of EAF requires a multidisciplinary team involving surgeons, nursing wound care and nutritionist. The objectives of EAF treatment are control of intestinal effluent, limiting the exposure of surrounding viscera and granulation tissue, eliminating infection, and achieving the best physical condition before definitive reconstructive surgery. However, the major treatment particularities of EAF are the effluent control difficulties and complexity of reconstructive surgery. Once EAF is diagnosed, the control of sepsis and fluid resuscitation constitute the priority because these patients may have already a protein loss with frequently sepsis from localized wound infection or abdominal deep abscess . The first step in presence of EAF is to eliminate deep abdominal sepsis and an unrecognized concurrent deep EAF. Abdominal CT scan should be performed as soon as possible after EAF diagnosis to exclude intra-abdominal sepsis, if present; the sepsis should be drained with radiological assistance [29,30]. Importantly, the second step is to define the fistula mapping and evaluate how much contiguous bowel is available for eventual introduction of enteral nutrition . To achieve this goal, some investigations such as fistulography and oral dye ingestion (as bleu methyl) may be more helpful when used in combination with a CT scan .
EFFLUENT CONTROL/SKIN PROTECTION
Controlling the effluent, protecting the exposed bowel, the granulation tissue and the skin surrounding fistula from erosion, inflammation and potential infection should be planned very early to limit consequences. A poorly controlled EAF constitutes a source of embarrassment and discomfort for the patient and frustration for the medical team. Subsequently, it results in the consumption of a tremendous amount of nursing and disposable medical resources. The intestinal content is very corrosive, so early the control of EAF output is critical to limit skin damage that may limit options for subsequent control. The first step is to stop oral intake and bowel rest decreases the fistula output significantly. The second step is to use techniques that allow fistula effluent control and protection of the surrounding tissue and skin. Several methods and systems have been developed to achieve effluent control and skin protection [31-35]. Agents such as cellular dermal matrix and fibrin glue have been used to attempt local fistula closure; however, the failure in clinical practice was due to the moisture and continuous intestinal peristalsis . Also performing local extra peritoneal repair of fistula hole followed by split-thickness skin graft to cover the exposed bowel to transform thus EAF to stoma has been described with limited clinical success . Creation of a “floating stoma” which consisted of suturing the perforated wall bowel to a plastic silo piece with a hole in it, allowing separation of draining intestine from the peritoneum beneath it . This technique has been reported to be useful in specific circumstances particularly in case of deep EAF .
The techniques combining negative-pressure wound management systems with ostomy appliances are more promising with the objective to control fistula effluent, allow granulation of the surrounding tissue, protection of skin and prevention of underlying bowel from trauma [34,39,40]. The original technique initially described by Goverman et al.  consisted of covering the open area and exposed bowel and applying a negative pressure system to the dressing. So the open abdomen area is covered with a thin layer of impregnated gauze with a hole cut out for fistula opening. In a similar fashion, sponges with a hole to accommodate the fistula opening and then a polyurethane drape is placed. Once placed, a hole is cut on the drape and an ostomy appliance or catheter is placed over or within the fistula opening, and then the negative pressure is applied to the entire dressing. Over the years, a few modifications have been added to the original technique. As demonstrated by published reports, the negative pressure wound therapy system (NPWT) is very useful to control EAF output and to protect and improve surrounding granulation tissue healing (Figure 2) [42,43]. However, the involvement of the stoma therapist or an experienced wound care team is highly required . The wound care team is more familiar with the akin protection materials such as stoma paste and powder which should be used early. Stoma paste and powder can be used to improve isolation of the fistula. In absence of these care resources, transfer to high-level care should be considered. More recently, negative pressure wound management system has been adapted and used to control the effluent and stop ongoing peritoneal contamination in deep EAF [44,45]. “Floating stoma” method has been used to control deep effluent and limit peritoneal diffusion of infection . As a reminder, deep EAF with an open abdomen is a surgical emergency in critically illness situation. The goal of surgery is to strictly achieve drainage control of digestive content and to transform such fistula to superficial EAF without an attempt to perform any sort of surgical fistula procedure. Therefore performing fistula surgery in such case can result in increasing intestinal wall defect and aggravating already complicated clinical situation because of bowel edema, mesenteric shortening, and vascularized adhesions . There is no specific system designed for the purpose of EAF, however, considerable efforts of the care team are required to design a custom device for a patient with EAF and to ensure its effective use on a daily basis. Once the surrounding tissue granulation is achieved, the granulating area is covered by a split-thickness skin graft and thus EAF is managed much likely as a conventional stoma until the time of fistula and abdominal wall reconstructive surgery.
The introduction of early nutrition is the key of success in a patient with EAF. Nutritional troubles are present in 50% to 90% of patients with an ECF and contribute significantly to the overall morbidity and mortality [46,47]. Therefore adequate nutrition is essential for these patients to achieve an acceptable nutritional condition. The goal of nutrition support in patients with EAF is to prevent malnutrition while controlling fistula effluent and not to promote fistula closure . Therefore immediately upon diagnosis, correction of fluid and electrolyte imbalances is required to normalize acid-base balance and quit the inflammatory process. The fluid needs can be very high in the early phase depending principally on the GI tract losses and secondarily on losses due to sepsis and fever. However, the GI tract losses can vary widely depending on the site of EAF. When fistula site is on the proximal jejunum, the fluid losses are important and so knowledge of GI fluids composition is necessary to effectively treat and prevent abnormalities (Table 1). The development of PN was the most important advances made in ECF management. The PN should be introduced as soon as the EAF diagnosis has been established and the patient had been resuscitated and sepsis treated. The purpose of nutrition support is to meet the patient metabolic needs while definitive management is planned [5,48]. The high fistula output and fluid losses from an open abdomen should be taken into consideration when calculating the patient nutrition needs. Up to 75 g/d of protein is normally absorbed by the small bowel . The fluid loss from open abdomen contains up to 2 g of nitrogen per litter and so it should not be underestimated . The calorie and protein needs may reach kcal/kg/d and 1.5-2.5 g/kg/d in case of a high-output fistula . However, care should be taken to avoid overfeeding consequences. Supplementation in copper, folic acid, vitamin B12 and C and trace minerals may be necessary for a patient with long-standing small-bowel fistulas . As shown, the spontaneous fistula closure rate was doubled after nutritional supplementation addition [1,48,50]. However, the heterogeneity of population involved in the studies and the predominance of the retrospective nature of these studies made more difficult to predict accurately the timing and rate of spontaneous healing [1,48]. As suggested by some studies, the fistula closure rates and mortality have been positively affected by PN  but until to date, there is no strong evidence that ECF closure is increased with PN alone . Although in some cases, PN may be the only nutritional support that patient tolerates, enteral feeding is possible in large series of patients with ECF [53,54]. Enteral nutrition should be attempted once the fistula anatomy is defined and feasibility of enteral feeding is determined by the management team. The enteral nutrition is beneficial by preserving the mucosal barrier and immunologic function of the intestine resulting in decreasing infectious complications. The absolute contraindication to enteral nutrition is insufficient length (usually <75 cm) of usable bowel. The quality of the remaining small bowel is also important. The length of usable bowel can be difficult to estimate, however upper GI series, magnetic resonance enterography and CT scan are useful to make a reasonable estimation. Enteral nutrition can be administrated by surgical tube-jejunostomy, a passage of tube distal to fistula and fistuloclysis. However, establishing enteral feeding access can be difficult in some cases and teamwork perseverance is required in these circumstances . Fistuloclysis is a technique which consists of providing an enteral feeding through the fistula opening. The fistula effluent is collected from the proximal fistula limb and reinstilled into the distal limb. This is very useful to maintain fluid and electrolyte balance. Fistuloclysis technique can be used to introduce enteral nutrition by inserting a tube through the distal intestinal limb and the tube must be maintained in a stable position avoiding migration and obstruction. Feeding a patient with EAF is reasonably started with standard polymeric formula. Exceptionally, if the usable bowel has a very short length less than 120 cm and the patient does not tolerate the polymeric formula or experiences high fistula output, the patient should be switched to an elemental or semi-elemental feed. As reported, the use of fistuloclysis with polymeric or elemental feeds resulted in patients with ECF resulted in the liberation of an important number of them from PN .
The introduction of Immunonutrition (glutamine) in critically ill surgical patients showed a reduction in infectious complications without effect on mortality . Glutamine which is the primary nitrogen constitutes an energy source for the enterocyte and has a large effect on immune function and overall outcomes . Glutamine has more pronounced positive effects when it is administrated parenterally . As reported, the combined use of oral glutamine with PN in high output fistula had been associated with accelerating healing and decreasing mortality without change in hospital stay length . However regarding the limit data in the EAF patients, the administration or oral glutamine in the hope to decrease overall inflammation and fistula effluent seems to be probably safe.
Somatostatin is a hormone principally produced by the delta cells of the pancreas. Somatostatin and its analogues (octreotide) have an inhibitory properties including decrease of enteric secretions, suppression of gastrointestinal hormones, reducing of gastric emptying rate and having a splanchnic vasoconstrictive effect [59,60]. Based on these inhibitory properties, the use of somatostatin has been advocated in the treatment of ECFs to reduce the fistula output volume . Oppositely to somatostatin which has a short half-life (1-2 min) requiring continuous infusion , Octreotide is a longer-acting analogue with a half-life of 113 min allowing intermittent subcutaneous dosing and it has wide use in ECFs treating . The efficacy of this medication has been evaluated by measuring the impact on the fistula output volume, time to closure and fistula closure rates. As demonstrated by investigations, both somatostatin and octreotide have an effective effect in decreasing the fistula output volume by as much as 40%-93% . This reduction in output would be very beneficial in improving quality of life and prognosis of a patient with high output fistula volume by facilitating wound care and decrease damage to bowel and surrounding granulation tissue [60,62]. The combined use of TPN with somatostatin has a synergistic effect on the reduction of intestinal secretions and the improvement of fistula closure rates . Several controlled trials demonstrated the significant improvement of these medications on the time to closure of ECFs [62-65].
On the other hand, most reports showed no effect on the actual rate of closure after use of somatostatin and its analogues [59,65]. This may be interpreted as a failure of conservative treatment which can be more likely related to fistula nature, such as its location, presence of a distal obstruction or malignancy. In addition, the octreotide can have an adverse effect on immune function and can reduce the splanchnic and portal blood flow . So care must be taken when using this medication. The use of Proton pump inhibitors and H2 receptor antagonists did not show any positive effect on the fistula output and the spontaneous closure rate [3,10].
Timing of surgery: Defining the appropriate time to perform definitive reconstructive surgery for EAF after the failure of conservative treatment is unclear in the absence of level I data supporting any specific period of delay. The timing of reconstructive surgery for EAF and AWR should be individualized according to patient characteristics. Softening of intra-abdominal adherences, resolution of inflammatory processes and abdominal sepsis, achieving a best nutritional condition of the patient, providing adequate wound care and reduction in the risk of bowel injury take more time usually longer than 3 months before conditions become ideal for surgery. Therefore, the surgical judgment based on these multiple factors is likely the key to success. The longer time interval to surgery is associated with lower rates of fistula recurrence, morbidity and mortality [67-74]. So at least a waiting period of 6 months or longer after fistula formation is highly recommended by specialized centre authors [71-74].
The risk factor that it can be modified is the surgical technique. Bowel resection was superior to over sewing and wedge repair, and complete resection of the affected intestinal segment was associated with lower rates of fistula recurrence [67,72,75]. The preferred anastomosis technique between stapled and hand-sewn types is not well defined due to the lack of published studies comparing these two techniques. However, the stapled anastomosis was found to be a significant risk factor for fistula recurrence and one-year mortality [72,75]. Based on experience, the gastrointestinal surgeons believe that hand-sewn anastomosis is superior to stapled anastomosis in fistula surgery.
Abdominal wall reconstruction
The EAF is associated with an abdominal wall defect and reconstructive surgery is needed in most cases. However, reconstruction of the abdominal wall is a complex and high-risk procedure. When performing definitive surgery for EAF, all efforts should be made to obtain closure of the abdomen over the bowel avoiding exposition to the environment which is the leading factor to EAF formation. The decision to stage the repair or not influences in part the choice of the abdominal wall closure approach. There is no ideal technique or a simple approach to abdominal wall reconstruction (AWR). However, it is so important to take into consideration the patient functional status and expectations in determining the appropriate approach for AWR. Simple mesh underlying fascial defects closure is an acceptable hernia repair. However, the patient is left with a large area of laxity on the anterior abdominal wall resulting in limitation of patient physical activities in future with less cosmetic appearance. Component separation techniques (CST) and flap reconstructions can provide a functional AWR. However, these techniques are more demanding and they are associated with increased wound complications. The original CST consists of separating the rectus muscle from its posterior sheath and the external oblique muscle from the internal oblique muscle allowing medial advancement of approximately 5 cm at the epigastrium, 10 cm at the waistline and 3 cm in the suprapubic region unilaterally [76,77]. So, the ideal use of CST is in facilitating the reapproximation of rectus complex to the midline. The reported rates of hernia recurrence after CST varied from 6% to 52%. [77-82]. However, very large abdominal wall defects are more likely to require mesh-bridging techniques even following CST procedure. When the CST procedure is reinforced with mesh placement, it perfectly restores a dynamic and functional abdominal wall. Compared to simple CST, prosthetic mesh closure is more frequently associated with wound complications, and recurrence rates were similar in the two methods . Several minor modifications have been introduced on to the original CST technique with good results [81,82]. The retrorectus space has been exploited for placement of mesh reinforcement and many major proponents of the classic anterior CST have shifted to the posterior approach [81-83]. As demonstrated by CT scans performed in preoperative and postoperative setting following large abdominal wall hernias repair, the use of CST resulted in a significant increase of the intra-abdominal volume without pulmonary compromise . So restoring the lost domain may be possible after CST use without respiratory repercussions related to the loss of thoracic volume. The major inconvenient of the anterior CST is large bilateral skin flaps resulting from necessary dissection for exposure and flap complications were the most wound matter noted in this procedure. The seroma and potential infection are common after performing anterior CST. The use of fibrin sealant has been shown to decrease seroma and wound infection rates . Also eliminating the dead space by performing numerous “quilting” mattress sutures has been reported to reduce seroma formation. The use of the minimally invasive technique has been described to achieve lateral release by creating small tunnels from the midline incision instead of large flaps . Although the use of a large midline incision approaches with avoiding creating a large flap with their attendant wound morbidity, this technique is the ideal method for a single stage repair of EAF . Therefore, laparoscopic and minimally invasive approaches are likely useful to achieve a functional abdominal wall with avoiding morbidity related to extensive open procedures [86-88].
Enteroatmospheric fistula (EAF) is a feared and challenging complication for the clinical team. The open abdomen (OA) is associated with high risk of EAF formation. The multidisciplinary approach is the key to successful management. The principles treatment is based on the patient resuscitation, the elimination of abdominal infection, the control of fistula effluent, the wound care and the introduction of nutritional support. The spontaneous healing of EAF is extremely rare and definitive surgery should be postponed until obtaining the best physical condition of the patient. The abdominal wall reconstruction is a complex and high-risk surgery. The abdominal wall repair can be staged or concomitantly performed with fistula surgery. Several factors may influence the determination of the appropriate wall closure approach. However, the prevention remains the best way to reduce the risks of EAF.
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