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Surgical Techniques and Differences in Postoperative Outcomes for Patients With Crohn’s Disease With Ileosigmoid Fistulas

A Single-Institution Experience, 2010–2016

Fennern, Erin M.D., M.P.H.1; Williamson, John M.D.2; Plietz, Michael M.D.1; George, Justin M.D.1; Khaitov, Sergey M.D.3; Greenstein, Alexander J. M.D., M.P.H.3

doi: 10.1097/DCR.0000000000001451
Original Contributions: Inflammatory Bowel Disease
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BACKGROUND: Surgical treatment of ileosigmoid fistulas in Crohn’s disease is poorly characterized.

OBJECTIVE: The purpose of this study was to identify differences in patient postoperative outcomes for isolated ileosigmoid fistulas by surgical approach (laparoscopic versus open) and sigmoid colon repair type (sigmoid resection versus primary repair).

DESIGN: Using a prospectively collected database, we gathered perioperative data from chart reviews to calculate differences and associations between treatment groups.

SETTINGS: The study was conducted at a single tertiary care center.

PATIENTS: Patients with Crohn’s disease who underwent surgery for isolated ileosigmoid fistulas between July 1, 2010, and June 30, 2016 were included.

RESULTS: We identified 84 patients, with an average age of 37 years. A total of 51 were men and 33 were women; 34 underwent a sigmoid resection, whereas 50 had a primary repair of the sigmoid. All of the patients underwent an ileocolic resection. A total of 67 surgeries were initially attempted laparoscopically, of which 17 (25.4%) were converted to open, with 50 (59.5%) completed laparoscopically. There were no significant differences in length of stay or incidence of postoperative complications by surgical approach (laparoscopic versus open). For patients who underwent a primary sigmoid repair versus a sigmoid resection, there were no significant differences in postoperative complications, but there was a significant difference in the length of stay (6.36 vs 9.56 d for primary repair versus resection; multivariate p value of 0.022).

MAIN OUTCOME MEASURES: Postoperative complications and length of stay were measured.

LIMITATIONS: The study was limited by its small sample size, cross-sectional nature of the data, and limited information about preoperative outpatient medical treatment.

CONCLUSIONS: Laparoscopic surgery for isolated ileosigmoid fistulas in Crohn’s disease is safe and does not result in a different length of stay or incidence of postoperative complications. Primary repair (rather than resection) of the sigmoid colon in these cases, when feasible, appears to be safe and is likely to be cost-effective given the reduced length of stay. See Video Abstract at http://links.lww.com/DCR/A993.

TÉCNICAS QUIRÚRGICAS Y DIFERENCIAS EN LOS RESULTADOS POSTOPERATORIOS PARA LOS PACIENTES CON ENFERMEDAD DE CROHN CON FÍSTULAS ILEO-SIGMOIDEAS: UNA EXPERIENCIA EN UNA SOLA INSTITUCIÓN, 2010-2016 ANTECEDENTES:

El tratamiento quirúrgico de las fístulas ileo-sigmoideas en la enfermedad de Crohn está mal caracterizado.

OBJETIVO: Identificar las diferencias en los resultados postoperatorios de los pacientes para las fístulas ileo-sigmoideas aisladas por abordaje quirúrgico (laparoscópica versus abierta) y tipo de reparación de colon sigmoide (resección sigmoidea versus reparación primaria).

DISEÑO: Utilizando una base de datos recopilada de forma prospectiva, se recopilaron datos perioperatorios de las revisiones de los gráficos para calcular las diferencias y las asociaciones entre los grupos de tratamiento.

AJUSTE: Un solo centro de atención terciaria.

PACIENTES: Pacientes con enfermedad de Crohn que se sometieron a una cirugía para fístulas ileo-sigmoideas aisladas entre el 1 de julio de 2010 y el 30 de junio de 2016.

RESULTADOS: Se identificaron 84 pacientes, con una edad promedio de 37 años. Un total de 51 eran hombres y 33 mujeres; 34 se sometieron a una resección sigmoidea, mientras que 50 tuvieron una reparación primaria del sigmoide. Todos los pacientes fueron sometidos a resección ileocólica. Inicialmente, un total de 67 círugias se intentaron por vía laparoscópica, de las cuales 17 (25,4%) se convirtieron en cirugías abiertas, y 50 (59,5%) se completaron por vía laparoscópica. No hubo diferencias significativas en la duración de la estancia o la incidencia de complicaciones postoperatorias por abordaje quirúrgico (laparoscópica versus abierta). Para los pacientes que se sometieron a una reparación sigmoidea primaria versus una resección sigmoidea, no hubo diferencias significativas en las complicaciones postoperatorias, pero sí hubo una diferencia significativa en la duración de la estancia hospitalaria (6,36 versus a 9,56 días para la reparación primaria frente a la resección; p multivariable -valor de 0.022).

PRINCIPALES MEDIDAS DE RESULTADOS: Complicaciones postoperatorias y duración de la estancia.

LIMITACIONES: Tamaño de muestra pequeño, naturaleza transversal de los datos e información limitada sobre el tratamiento médico ambulatorio preoperatorio del paciente.

CONCLUSIONES: La cirugía laparoscópica para fístulas ileo-sigmoideas aisladas en la enfermedad de Crohn es segura y no ocasiona una duración diferente de la estancia hospitalaria ni una incidencia diferente de complicaciones postoperatorias. La reparación primaria (en lugar de la resección) del colon sigmoide en estos casos, cuando es posible, parece ser segura y es probable que sea rentable, dada la duración reducida de la estancia. Vea el Resumen del Video en http://links.lww.com/DCR/A993.

1 Mount Sinai Hospital, New York, New York

2 Drexel University, Philadelphia, Pennsylvania

3 Department of Surgery, Mount Sinai Hospital, New York, New York

Funding/Support: None reported.

Financial Disclosure: None reported.

Poster presentation at the American College of Surgeons Clinical Congress Meeting, San Diego, CA, October 22 to 26, 2017.

Correspondence: Erin Fennern, M.D., M.P.H., 1 Gustave L. Levy Pl, New York, NY 10029. E-mail: Erin.Fennern@gmail.com

Entero-enteric fistulas are a common complication of Crohn’s disease (CD) and are often associated with greater disease severity.1 One large case series estimated the prevalence of internal fistulizing disease at 6% for all patients with CD and, of those, 19% possessed fistulas from the ileum to the sigmoid colon.2

The presence of an ileosigmoid fistula (ISF) is not a hard indication for surgical intervention.2 Most ISFs are asymptomatic and do not require urgent treatment; however, there is evidence that over time, progressive obstructive symptoms secondary to ileitis and scarring can occur. In addition, enlargement of the fistula can result in the bypassing of ileal contents into the distal colon, giving rise to debilitating diarrhea.3,4 In 1 case series that followed 36 cases of known ISFs, 31 required surgical intervention within 5 years of follow-up because of progressive symptoms.5

Descriptions of the surgical management of ISFs date back to 1974.4 Surgical management has evolved, as has the characterization of emerging surgical approaches,6–12 but gaps in knowledge remain.

In ISFs, the inflamed terminal ileum most commonly adheres and fistulizes to the sigmoid colon, which is often otherwise healthy. Because of this, surgical approaches to the sigmoid end of the fistula can involve either en bloc resection (Fig. 1) or simple division across the fistulous tract, using either sharp dissection or a stapler, with resection of only the diseased ileocolic segment (Fig. 2). Small case series indicate that perhaps >75% of ISFs can be managed with the latter approach,1,3,13 with sigmoid resection becoming necessary only when it is believed that primary closure of the fistula is at high risk of poor healing, that is, in cases with very wide fistulous tracts or active sigmoid disease. Little is known, however, about the differences in outcomes between these 2 surgical approaches.

FIGURE 1

FIGURE 1

FIGURE 2

FIGURE 2

Studies of laparoscopy in CD show that this surgical approach is associated with a more rapid recovery of bowel function, shorter hospital stay, a possible small decrease in 30-day postoperative complications, a decreased rate of clinically significant adhesions, and lower rates of incisional hernias.14,15 However, laparoscopy has not been examined specifically in the treatment of complex fistulizing CD, and no known published studies have examined rates of postoperative complications by surgical approach (laparoscopic versus open) for patients with isolated ISFs.16 The primary aim of this study was to identify differences in patient postoperative outcomes for isolated ISFs by surgical approach (laparoscopic versus open) and sigmoid colon repair type (sigmoid resection versus primary repair).

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PATIENTS AND METHODS

Institutional review board approval was obtained from the Icahn School of Medicine at Mount Sinai Hospital. Using a prospectively collected database of consecutive colorectal cases for 9 surgeons at Mount Sinai Hospital in New York City, we conducted a search of all bowel resections conducted from July 1, 2010, to June 30, 2016, for patients with a diagnosis of CD. Patients were included if they were >18 years of age at the time of the index operation, with a CD diagnosis (based off of International Classification of Diseases Ninth Revision and Tenth Revision codes), and an isolated ISF (determined via the operative report). Patients with other entero-enteric or entero-vesicular fistulas were excluded. Those with coexistent perianal fistulas were not excluded.

Thorough chart reviews were conducted for each case. Preoperative patient variables, including patient age, sex, and BMI, were included. These, as well as patient smoking status, were obtained from the preoperative anesthesia record. In addition, by reviewing both the preoperative clinic notes and the anesthesia records, we were able to calculate the Harvey Bradshaw Index (HBI) for each patient, a validated measure of CD severity based on patient-reported symptoms and physical examination findings.17,18 Examination of operative notes allowed us to extract whether surgeries were approached open or laparoscopic (the latter with a maximum extraction site length of 5 cm), as well as which cases were later converted to open. In addition, we determined whether the sigmoid appeared in the operating room to have signs of active disease, how the sigmoid end of the fistula was repaired (either resected or primarily repaired, the latter either with a stapler or handsewn), and whether a stoma was formed. Lastly, we carefully extracted information from the electronic medical chart regarding preoperative imaging and diagnostics, postoperative complications and/or readmissions, index length of stay (LOS), and perioperative treatment with steroids.

Our primary outcomes of interest were 30-day postoperative complications and index length of hospital stay (in days). Our primary predictor variables were operative approach (laparoscopic versus open operations) and type of sigmoid repair (primary repair versus en bloc resection).

We conducted both univariate and multivariate regression analyses to look for significant differences in the LOS and in the incidence of postoperative complications by Clavien-Dindo classification, the latter of which was dichotomized into minor (1 or 2) or none versus major (3 or 4) complications. Additional independent variables included age, sex, BMI, HBI, smoking status, and perioperative steroid use.

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RESULTS

We identified a total of 84 patients who underwent operations for isolated ISFs by 9 different surgeons at Mount Sinai Hospital from July 1, 2010, to June 30, 2016. These isolated ISF cases were identified via chart reviews of the approximately 1500 bowel resections for CD performed by the surgeons at Mount Sinai Hospital included in our case series. (Of note, there were approximately 150 cases of ISFs with coincident entero-enteric fistulas occurring during this time period.) Two of the surgeons accounted for 51 of the 84 surgical ISF cases. All 9 of the surgeons contributed laparoscopic surgeries. The average age of patients was 37 years. Fifty-one were men, and 33 were women. The only statistically significant difference (p < 0.05) in patient characteristics was that a larger proportion of patients who underwent a primary sigmoid repair received stress-dosed steroids compared with those patients who underwent sigmoid resection (Table 1).

TABLE 1

TABLE 1

Of note, the outpatient records for most patients’ preoperative care were incomplete. Many patients saw gastroenterology providers outside of the Mount Sinai Health System, such that inclusion of preoperative CD medications in the generation of the disease severity scores was not possible. As a proxy measure, we examined the inpatient record and noted whether the patient received steroids during their index stay. This measure was included as a covariate in our multivariate model.

A total of 67 surgeries were initially attempted laparoscopically, of which 17 (25.4%) were converted to open. Overall, 50 of the 84 surgeries were completed laparoscopically, and 34 were completed open (Table 2).

TABLE 2

TABLE 2

Overall, 59 patients (70.2%) were diagnosed with ISFs preoperatively on imaging or colonoscopy. Of those, 49 were initially attempted laparoscopically; however, 16 of these patients were subsequently converted to open. Only 1 patient without a preoperative diagnosis of an ISF underwent an initially laparoscopic operation requiring conversion to open.

A total of 50 patients were treated with primary repair of the sigmoid, whereas 34 underwent a sigmoid resection. All 31 patients with signs of active CD of the sigmoid colon underwent a sigmoid resection. The remaining 3 sigmoid resections were performed for either strictures (n = 2) or excessive scar tissue, making a primary repair too difficult (n = 1).

LOS was limited to the index admission, with readmission treated as a complication. Forty-three patients (51.2%) experienced no postoperative complications. Thirty-three patients (39.3%) experienced a minor complication, with ileus being the most common. Eight patients (9.5%) experienced a complication requiring readmission, intervention, or an inpatient ICU stay. There were 5 patients who experienced anastomotic leaks (4 of which occurred at the ileocolic anastomosis and 1 at the sigmoid) and no deaths (Table 3).

TABLE 3

TABLE 3

Laparoscopy was analyzed first as an intention-to-treat variable and then by final approach. No significant differences were found between the 2 analyses. The final surgical approach was used in the analysis presented here.

In our univariate regression analysis, there were no significant differences in the incidence of postoperative complications by surgical approach or sigmoid repair type, nor was there a significant difference in the LOS by surgical approach (Table 4). There was, however, a significantly increased LOS for patients who underwent a sigmoidectomy as opposed to those who underwent a primary repair of the sigmoid (p = 0.009). These findings were mirrored in our multivariate analysis.

TABLE 4

TABLE 4

In our multivariate regression analysis, there were no significant differences in LOS or in the incidence of Clavien-Dindo postoperative complications for patients with laparoscopic versus open surgeries (Table 5). There were also no significant differences in the incidence of postoperative complications for patients with a primary sigmoid repair versus a sigmoid resection (Table 6). There was, however, a significant decrease in the LOS seen for patients who underwent a primary sigmoid repair as opposed to a sigmoid resection (6.36 vs 9.56 d for primary versus resection repair; multivariate p = 0.035).

TABLE 5

TABLE 5

TABLE 6

TABLE 6

A total of 10 patients received diverting loop ileostomies (Table 2). A subanalysis excluding these patients resulted in nearly identical findings with regard to LOS and incidence of postoperative complications. Stoma creation was significantly more likely in patients who underwent dual resections (both ileocolic and sigmoid) as compared with those who underwent ileocolic resections with sigmoid primary repairs (p = 0.017). In addition, 7 of the 10 patients who underwent a stoma creation were diagnosed with an ISF preoperatively; however, knowing the diagnosis preoperatively did not significantly correlate with the decision to divert.

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DISCUSSION

Descriptions of surgical management of ISFs dates back to 1974, when surgical approaches to ISFs were first described.6 The first patient series of 63 patients was drawn from a single-institution experience at Mount Sinai Hospital. In that article, the authors posited that the colon may be the origin of the fistula, accounting for why some patients get enterocolonic fistulas, versus others who experienced isolated enteritis or entero-enteric fistulas. With improvements in radiologic imaging and closer examination of pathologic specimens, we now know the colon to most often be an innocent bystander.19

In 1982, a series of 17 patients with CD with ISFs who underwent operations revealed that 13 of these patients were accurately diagnosed on radiologic imaging preoperatively.8 Using imaging (rather than intraoperative assessment), the authors concluded that all of the patients in this series did not have active Crohn’s colitis of the sigmoid. This series was the first to propose primary repair of the colonic end of the fistulous tract as an alternative to colonic resection.

In 1997, a retrospective cohort of 90 surgical cases of ISF repair found that patients were significantly more likely to undergo a sigmoid resection (as opposed to primary repair) if the ISF was found on preoperative radiology studies. Our study population (all of whom had a CT, a colonoscopy, or both) had a preoperative finding of an ISF diagnosed in 70% of patients (59 of 84 patients), which is consistent with other published reports in the recent past.11,12,19 Our study, however, did not identify a significant correlation between knowing the ISF diagnosis preoperatively and the procedure performed for repair of the sigmoid. A total of 25 (42%) of the 59 patients with an ISF diagnosed preoperatively underwent a sigmoid resection versus 8 (32%) of the 25 patients who did not receive an ISF diagnosis until they were in the operating room (p = 0.38). It seems unlikely that knowing the diagnosis preoperatively influenced the surgeon’s decision-making regarding the sigmoid repair technique.

Although only borderline statistically significant, this same study from 1997 also found a small difference in LOS by sigmoid repair type (8.3 d in the primary repair group versus 9.9 d in the resection group; p = 0.15). In addition, 7 patients in this group (8%) were found to have coincident colovesicular fistulas. Our study omitted patients with colovesicular fistulas and found a statistically significant increase in the LOS for patients who underwent double resections.

Two previous studies have attempted to examine CD-specific risk factors for conversion from laparoscopy to an open surgical approach,20,21 and although both of these studies showed increased conversion rates of 9% in cases of complex entero-enteric fistulas, as compared to 3% seen overall, neither study concluded that ISFs are a contraindication to attempted laparoscopy.22

A 2009 study at our institution examined the safety of laparoscopy in 335 laparoscopic bowel resections for CD dating back to 1993. Of these, 117 were found to have entero-enteric fistulas, with 51 found to have ISFs. It was determined that internal fistulizing disease could be managed by experienced laparoscopic surgeons safely, with acceptable morbidity.23 (Although our study looks at cases performed by surgeons included in this study, the cases are unique and were drawn from a later time period.) Subsequent studies further validated these findings.15,16,22

In our study, we found that a preoperative diagnosis of an ISF on imaging was significantly correlated with converting to an open operation and with the creation of a diverting stoma. Interestingly, only 1 patient without a preoperative diagnosis of an ISF underwent laparoscopy requiring a conversion to an open operation. (Of note, there was no significant difference in the presence of active sigmoid disease observed in the operating room between those patients with a preoperative diagnosis of an ISF versus those without.) This may indicate that ISFs detectable on imaging or colonoscopy are reflective of more severe disease of the terminal ileum or that knowing about an ISF preoperatively may have changed surgical decision-making in a way that is not fully understood.

Moreover, our finding that LOS was not significantly different for the laparoscopic versus the open operation group should be thoughtfully considered. The value of laparoscopy is not limited to LOS. Additional benefits, including decreased adhesions and the lower likelihood of subsequent incisional hernia, should still be considered when deciding on a surgical approach. In addition, given the small number of procedures in our series performed via a laparotomy, the lack of a significant difference in LOS or postoperative complications in our study may be attributed to limited statistical power.

In one other series of 104 ISFs from 2000 to 2007, >37% of these patients had coincident internal fistulizing disease requiring additional surgical resections. The authors found that postoperative complications did not differ by surgical approach (laparoscopic versus open) or by sigmoid repair type (primary repair versus resection).12 This series, however, likely experienced significant confounding, given the inclusion of patients with additional internal fistulizing disease. In this series, only 3 of 10 surgeons included performed laparoscopy. In our series, all 9 of the surgeons performed or attempted laparoscopic ISF repair. Only 19% of cases were completed laparoscopically versus 60% in our series, and 51% of the patients in this previous series received a diverting/protective stoma versus 12% in our series. These dramatic differences in surgical approach may reflect the multiple internal fistulas seen in many of these patients (37%) in the former series, indicating that inclusion of synchronous fistulas in a case series intended to analyze ISFs may have introduced significant confounding.

Our study of 84 patients with isolated ISFs contributes to the literature on the surgical management of CD by examining differences in postoperative complications by surgical approach and sigmoid repair type for patients with isolated ISFs and by adjusting for the effect of each surgical variable on the other in a multivariate analysis. These patients experienced no significant differences in the incidence of postoperative complications by operative approach (laparoscopic or open), nor by sigmoid repair type (primary repair versus en bloc resection). Nor did they have a significantly different LOS depending on whether they had an open or a laparoscopic operation. Patients in the series did, however, experience a significantly longer LOS when their sigmoid colon was resected rather than primarily repaired.

Given these findings, we advocate for performing a sigmoid primary repair in ISF cases, when feasible. This decision should be based on the surgeon’s ability to differentiate between diseased versus secondarily involved loops of bowel. If the sigmoid appears diseased, it should generally be resected along with the ileocolic segment. If, however, the sigmoid colon appears to be an innocent bystander, we would advocate for a primary repair, using either a handsewn or stapled primary closure. It should be noted, however, that in cases where the sigmoid does not appear diseased but there is either a large defect or a large abscess (particularly when on the mesenteric side of the bowel), the surgeon may appropriately decide to perform a segmental sigmoid resection. With regard to the decision to perform a diversion, a recent study showed a strong correlation between previous resections for CD and the risk for clinical anastomotic leak,24 suggesting that previous resection should be one variable taken under consideration. The decision, however, should be left up to the surgeon and made in the context of other factors, including patient nutritional status and intraoperative assessments of tissue integrity (Fig. 3).

FIGURE 3

FIGURE 3

Our analysis has several limitations that are important to consider. Given the cross-sectional and observational nature of the data, it is not possible to draw conclusions about causation. We are able to deduce associations, but hypotheses remain for why these differences exist. Specifically, questions about surgical decision-making remain unanswered–does preoperative knowledge of an ISF change the surgeon’s threshold for converting from laparoscopy to laparotomy? How does a surgeon decide when a diverting stoma ought to be formed for these patients?

In addition, given the nature of physician and surgeon practice patterns and endoscopic mucosal resection use at Mount Sinai Hospital, the data on a patient’s preoperative disease severity and the degree of immunocompromise are limited. Although we were able to calculate HBI, this measure has been shown to have variable validity when compared with endoscopic findings of disease severity.18,25 As a proxy measure, we determined whether patients were treated with steroids postoperatively; however, this gives an incomplete picture of the severity of a patient’s disease and his or her perioperative substrate.

Our conclusion from these findings is not that they should direct operative management but that they may provide valuable information for counseling patients both before surgery and during their hospital stay. Operative management of the sigmoid colon should be left up to the discretion of the surgeon. In the event that a surgeon must perform en bloc resection of the ISF (ie, both ileocolic and sigmoid resection), that patient can anticipate a longer hospital stay (and recovery) but no increased risk of postoperative complications. In addition, if an en bloc resection is planned preoperatively, the surgeon may wish to also perform a diverting stoma, something that the patient should be counseled on preoperatively, when possible.

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CONCLUSION

Laparoscopic operations for ISF in CD are safe and do not result in an increased incidence of postoperative complications, as compared with open surgeries. Moreover, primary repair of the sigmoid colon when feasible appears safe, with no increase in postoperative complications relative to sigmoid resections and is likely to be cost-effective, given the reduced LOS.

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ACKNOWLEDGMENTS

The authors thank Jill Gregory for her illustrations.

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REFERENCES

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Keywords:

Crohn’s disease; Ileosigmoid fistulas; Surgical technique

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