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Near infrared perfusion assessment of gastric conduit during minimally invasive Ivor Lewis esophagectomy
The American Journal of Surgery xxx (2017) 1e4
Contents lists available at ScienceDirect
The American Journal of Surgery journal homepage: www.americanjournalofsurgery.com
Near infrared perfusion assessment of gastric conduit during minimally invasive Ivor Lewis esophagectomy Brian G.A. Dalton, Abubaker A. Ali, Marie Crandall, Ziad T. Awad* Department of Surgery, University of Florida Health- Jacksonville, United States
a r t i c l e i n f o
a b s t r a c t
Article history: Received 27 September 2017 Received in revised form 31 October 2017 Accepted 6 November 2017
Introduction: Anastomotic leak and conduit necrosis are devastating complications following Ivor Lewis esophagectomy. Near infrared imaging (NIR) using IndoCyanine Green allows for real time tissue perfusion assessment which may reduce anastomotic leak during minimally invasive Ivor Lewis esophagectomy (MIE). Methods: Forty consecutive MIE were performed by a single surgeon at a tertiary referral center. The first 20 were assessed for gastric conduit perfusion by clinical criteria (Group 1). The second 20 were also assessed using NIR laparoscopic system (Group 2). Results: Comparing Group 1 to Group 2, no significant differences were found in overall complication rate, readmission or reoperation rate. NIR resulted in resection of the non perfused proximal portion of the conduit in 30% (6/20). Two patients in group 2 group developed anastomotic leak (2/20) compared to 0 in Group 1 (p ¼ 0.49). Graft necrosis led to one mortality in Group 1, while there were 0 mortalities in Group 2. (p ¼ 1.0). Conclusion: Although NIR plays a role in assessment of tissue perfusion, in our study its use did not result in reduction of anastomotic leak rate. © 2017 Elsevier Inc. All rights reserved.
Keywords: Near infrared imaging Ivor Lewis esophagectomy Minimally invasive esophagectomy Indocyanine green angiography Anastomotic leak Graft necrosis
1. Introduction Esophagectomy is one of most invasive procedures in gastrointestinal surgery and despite improvements in surgical techniques and perioperative care, the mortality rate remains high.1 A study using the National Surgery Quality Improvement Program database (NSQIP) between 2006 and 2011 reported that the morbidity of patients with esophagectomy was 43.8% and mortality was 3.8%.2 In particular, anastomotic leak after esophagectomy remains an important cause of patient morbidity and impaired quality of life.3e5 In the majority of cases, reconstruction after esophagectomy is done using a gastric conduit that is perfused by the right gastroepiploic arcade. Perfusion at the proximal portion of the graft, in the area where the anastomosis is typically created, is variable but often tenuous because the gastroepiploic arcade rarely reaches the tip of the graft. Instead, the most proximal portion of the graft is typically perfused by intramural capillaries within the wall of the
* Corresponding author. Division of General and Gastrointestinal Surgery, University of Florida Health- Jacksonville, 653 West 8th Street, Jacksonville, FL 32209, United States. E-mail address: [email protected]fl.edu (Z.T. Awad).
stomach and small vessels in the omentum along the greater curvature.6 Historically, evaluation of the blood flow of the gastric conduit has been a challenge to most surgeons as relying on inspection of the color of gastric serosa is often inaccurate and misleading. Indocyanine green (ICG) fluorescence angiography and Doppler examination have recently been used to assess blood supply and assist in conduit construction. These modalities have been employed in an effort to reduce anastomotic complications after esophagectomy.6,7 The Near Infrared (NIR) laparoscopic system (PINPOINT Endoscopic Fluorescence Imaging System, NOVADAQ, Mississauga, ON, Canada) is used to provide high definition (HD) white light imaging during minimally invasive surgery (MIS), as well as NIR irradiation and ICG fluorescence emission imaging. This system provides a real-time false-color superimposition of ICG fluorescence signal on the HD white light view. This overlay allows simultaneous appreciation of dynamic perfusion and visualization of the conventional MIS video image. In theory, the PINPOINT system might provide valuable real-time information about perfusion of the gastric graft during minimally invasive Ivor Lewis esophagectomy (MIE) and this might influence
https://doi.org/10.1016/j.amjsurg.2017.11.026 0002-9610/© 2017 Elsevier Inc. All rights reserved.
Please cite this article in press as: Dalton BGA, et al., Near infrared perfusion assessment of gastric conduit during minimally invasive Ivor Lewis esophagectomy, The American Journal of Surgery (2017), https://doi.org/10.1016/j.amjsurg.2017.11.026
2
B.G.A. Dalton et al. / The American Journal of Surgery xxx (2017) 1e4
resection margins and surgical outcomes. The hypothesis is the use PINPOINT system during MIE esophagectomy would reduce anastomotic leak rates. 2. Methods After Institutional Review Board approval (IRB#201600651) a retrospective analysis of prospectively collected data of all MIE performed at our institution was performed. All MIE from April 2014 to January 2016 were included. All surgeries were performed for cancer and were performed by a single surgeon (ZA) at a tertiary referral center. Cases were analyzed in 2 groups. Group 1, the conduit was evaluated using standard clinical criteria by inspecting the color of the gastric serosa. Group 2, NIR technology was used intraoperatively for assessment of graft perfusion. Data is presented as mean ± standard deviation unless otherwise stated. Significance is defined as P 0.05. Comparative analysis was performed using student t test for continuous variables and Fishers exact for binary variables or Chi square test with Pearson correlation where appropriate.
Fig. 2. Gastric conduit after ICG injection on NIR with poor perfusion evident in proximal conduit. Line of perfusion demarcation (arrows) shown in PINPOINT modes.
3. Technique The abdominal portion of the procedure was performed laparoscopically. Dissection began by opening the gastrocolic omentum below the level of the pylorus, taking care to preserve the right gastroepiploic arcade. The right gastric artery was preserved in all patients. The greater curvature of the stomach was mobilized and the short gastric vessels are divided. The left gastric artery was dissected and transected using the vascular stapler after all nodal tissue is lifted off the celiac axis. A 5 cm wide gastric conduit (Fig. 1) was constructed using multiple firings of the laparoscopic linear stapler. Pyroloplasty was performed in all patients. The thoracic portion was performed thoracoscopically with the patient in the left lateral decubitus position. The inferior pulmonary ligament was incised and the right lung was retracted. The mediastinal pleura was incised and the esophagus was dissected to the level of the azygous vein, which was divided using the laparoscopic vascular stapler. The gastric conduit was pulled into the right chest, the specimen removed and end to end esophagogastric anastomosis was constructed intracorporeally using the mechanical circular stapler 25 mm DST XL EEA (Covidien, Newhaven, CT, USA). Beginning in February 2015, NIR assessment of conduit perfusion was done using the PINPOINT system - 7.5 mg of ICG is injected intravenously and conduit perfusion assessment is done 60 s after injection. A marking silk stitch was placed when there was a demarcation between the perfused and non-perfused part of the conduit (Fig. 2). The non-perfused segment was resected in the chest, and the anastomosis was constructed between the native esophagus and perfused proximal stomach.
Fig. 3. Gastric conduit after ICG injection showing good perfusion throughout conduit.
When the conduit appeared well perfused throughout (Fig. 3) a stitch was still placed on the anterior surface of the conduit for orientation purposes upon transposition into the chest. All patients underwent upper GI contrast study on day 4 prior to oral intake. Anastomotic leak was defined as full thickness defect of esophagus, conduit, anastomosis or staple line.8 Oral intake was started the day of upper GI contrast study if the study was negative for leak. 4. Results During the study period, 40 consecutive patients having undergone MIE. Group 1, 20 consecutive patients (April 2014eJanuary 2015). Group 2, 20 consecutive patients (February 2015eJanuary 2016) were NIR was used. The administration of ICG caused no adverse events in the NIR group. No differences were found between the 2 groups with regard demographic or preoperative parameters (Table 1).
Table 1 Demographic and preoperative date Group 1 vs Group 2.
Fig. 1. Tubularized gastric conduit.
Value
Group 1 (n ¼ 20)
Group 2 (n ¼ 20)
P value
Age (years) % Male BMI (kg/m2) % adenocarcinoma Neoadjuvant therapy (%) COPD (%) Coronary artery disease (%) Peroperative albumin (mg/dL)
66.2 ± 8 80 26.3 ± 4.1 70 95 20 15 3.9 ± 0.4
61.8 ± 12.8 80 26.4 ± 4.9 90 85 15 25 3.9 ± 0.4
0.2 1 0.97 0.24 0.6 1 0.69 0.69
COPD: chronic obstructive pulmonary disease.
Please cite this article in press as: Dalton BGA, et al., Near infrared perfusion assessment of gastric conduit during minimally invasive Ivor Lewis esophagectomy, The American Journal of Surgery (2017), https://doi.org/10.1016/j.amjsurg.2017.11.026
B.G.A. Dalton et al. / The American Journal of Surgery xxx (2017) 1e4 Table 2 Perioperative outcomes Group 1 and Group 2. Value
Group 1 (n ¼ 20)
Group 2 (n ¼ 20)
P value
Anastomotic leak (%) Graft necrosis (%) Length of stay (days) Overall complication rate (%) Reoperation within same admission (%) 90 day reoperation (%) 90 day readmission (%) 90 day mortality (%) Atrial fibrillation (%) Respiratory failure
0 5 8.1 ± 1.9 55 5
10 0 9.8 ± 4 40 10
0.49 1 0.09 0.53 1
15 20 5 25 10
15 10 0 25 0
1 0.66 1 1 0.49
All patients were diagnosed with esophageal cancer. There was no difference in operative time (371 ± 90 vs 379 ± 66 min, p ¼ 0.76) or estimated blood loss (159 ± 150 ml vs 338 ± 723, p ¼ 0.28) between the 2 groups. Mean blood loss and standard deviation (SD) in Group 2 was increased by the presence of one outlier (>2 SD outside the mean). This patient had an injury to an aberrant pulmonary vein branch which was controlled but the esophagogastrostomy was delayed until an operating room return 2 days later. This was also the only patient in the series to receive an intraoperative transfusion. No statistically significant differences were found between the 2 groups in overall complication rate, anastomotic leak, graft necrosis, reoperation or length of stay (Table 2). The use of NIR resulted in resection of proximal non-perfused proximal part of the conduit in 30% (6/20) of patients. The 2 leaks in the NIR were in the group that needed proximal conduit resection, and both leaks were managed with endoscopic stent placement. These endoscopic stents were placed in an elective fashion. In Group 1, 3 patients required surgical intervention within 90 days: one patient for wound infection required debridement at the jejunostomy site, one for cecal volvulus necessitating right colon resection, and the third patient was explored for graft necrosis. This patient underwent resection of the graft with cervical esophagostomy, and was the only mortality from either group. In Group 2, reoperation within 90 days were observed in 3 patients: one patient with conduit obstruction as a result of redundant conduit above the diaphragm, the patient with pulmonary vein branch injury described earlier, and one patient with post esophagectomy hiatal hernia. Ten total patients were diagnosed with postoperative atrial fibrillation. One of these patients required cardioversion (Group 2). One patient in the Group 1 was diagnosed with a Clostridium Difficile infection and was treated with antibiotics. Another patient in Group 1 developed colonic pseudo-obstruction and was treated non-operatively. 5. Discussion A large database study examining all modalities of esophagectomy showed overall major morbidity of esophagectomy to be 33.8% and anastomotic leak rate of 12.9%.9 Anastomotic leak has also been linked to increased morbidity in patients undergoing esophagectomy.10,11 Our study did not answer the question if NIR can reduce the anastomotic leak rate. Zehetner et al. using SPY Imaging System (Novadaq, Ontario, Canada) among patients undergoing open transhiatal esophagectomy showed a significantly higher leak rate (45% vs 2%, p < 0.0001) when the anastomosis was performed to an area of gastric conduit distal to the line of perfusion demarcation.6 Campbell et al. employed both Doppler and intraoperative ICG
3
fluorescence angiography- SPY Elite System (LifeCell, Bridgewater, NJ, USA) among patients undergoing Ivor Lewis esophagectomy.7 They adopted a quantitative perfusion cutoff of 75% as the area where the esophagogastric anastomosis was performed, usually 10 cm above the pylorus. The leak rate was 0% (30 patients) when the anastomosis was placed proximal to the 75% relative perfusion line compared to 20% leak rate (60 patients) prior to the use of either technology.7 In both studies,6,7 a midline abdominal incision is required to deliver the conduit to the outside for quantitative perfusion assessment using SPY System or intraoperative Doppler, while our approach is pure minimally invasive (laparoscopic and thoracoscopic). We did not use laparoscopic Doppler and relied solely on qualitative assessment of gastric conduit perfusion. If quantitative data were available with the PINPOINT system establishing a standardized level of perfusion necessary for successful anastomosis, this could play a role in reducing anastomotic leak rate. Degett et al. in a systemic literature review of ICG- FA (fluorescence angiography) to assess perfusion during construction of a primary gastrointestinal anastomosis showed the technique to be associated with reduced risk of anastomotic colorectal leaks compared with no ICG-FA.12 However, the anastomotic leakage rate in patients with esophageal anastomoses and intraoperative ICG-FA assessment was 14% (n ¼ 30/214). None of the studies involving esophageal anastomoses had a control group without ICG-FA assessment. They concluded that ICG-FA is a feasible and promising tool. However, heterogeneous studies and the lack of high level of evidence the clinical benefit of ICG-FA is inconclusive. Furthermore, the technique remains subjective until more objective cutoff levels for sufficient perfusion has been established.12 In our study, 6/20 (30%) of patients underwent resection of non-perfused proximal gastric conduit using the NIR, allowing a well-perfused gastric conduit to be consistently used for the esophagogastric anastomosis. It is concerning, however, that anastomotic leaks were observed in 2/6 (33.33%) patients in this group, and raises the possibility that proximal resection might have created undue anastomotic tension and compromised blood supply. Although tension is difficult to assess and quantify, especially when minimally invasive surgery is utilized, we routinely roll the anastomosis from side to side and lift it to examine the entire staple line; this maneuver would not be possible had the anastomosis being under tension. Is it unknown whether those patients with demarcation between the perfused and non-perfused part of the conduit using NIR are at risk of anastomotic failure, and proximal resection was a marker of a potentially higher-risk anastomosis. Other authors agree with our opinion that the intra-thoracic anastomosis provides the ability to resect the tip of the gastric conduit, and the anastomosis is not under excessive tension13 as the surgeon has control on the level of transection of the esophagus relative to the location of the esophageal cancer. Limitations of this study include small population, retrospective nature, single center and single surgeon, all of which introduce potential bias. However, to our knowledge, the present study is the first using the PINPOINT system for graft perfusion assessment among patients undergoing strict laparoscopic/thoracoscopic esophagectomy. Future directions of research include studying this modality of NIR using quantified perfusion values should they come available. We would hope to establish a level of perfusion that results in a negligible anastomotic leak rate. 6. Conclusion In our study, the use of NIR or interventions based on its findings did not result in reduction of anastomotic leak rate. Better quantitative integrated metrics are needed to better define tissue
Please cite this article in press as: Dalton BGA, et al., Near infrared perfusion assessment of gastric conduit during minimally invasive Ivor Lewis esophagectomy, The American Journal of Surgery (2017), https://doi.org/10.1016/j.amjsurg.2017.11.026
4
B.G.A. Dalton et al. / The American Journal of Surgery xxx (2017) 1e4
perfusion using the PINPOINT system. Further studies are warranted to validate the use of this novel technology. Conflicts of interest No conflicts of interest were encountered during this project by any of the authors. No external financial or material support was provided, and there are no commercial or financial interests related to the topic. Author contributions BD: Data collection, analysis, interpretation, manuscript drafting, critical revision AA: Study design, data collection, critical revision. MC: Interpretation, manuscript drafting, critical revision. ZA: Study design, data collection, analysis, interpretation, manuscript drafting, critical revision. All authors agree to the manuscript its submitted form and attest to the accuracy of the data and interpretation of the data. References 1. Saeki H, Masuda T, Okada S, et al. Impact of perioperative peripheral blood values on postoperative complications after esophageal surgery. Surg Today. 2010 Jul;40(7):626e631. 2. Lucas DJ, Pawlik TM. Quality improvement in gastrointestinal surgical oncology with American college of surgeons national surgical quality improvement Program. Surgery. 2014 Apr;155(4):593e601.
3. Fernandez FG, Meyers BF. Quality of life after esophagectomy. Semin Thorac Cardiovasc Surg. 2004;16(2):152e159. Summer. 4. Schuchert MJ, Abbas G, Nason KS, et al. Impact of anastomotic leak on outcomes after transhiatal esophagectomy. Surgery. 2010 Oct;148(4):831e838. discussion 838e840. 5. Kassis ES, Kosinski AS, Ross Jr P, Koppes KE, Donahue JM, Daniel VC. Predictors of anastomotic leak after esophagectomy: an analysis of the society of thoracic surgeons general thoracic database. Ann Thorac Surg. 2013 Dec;96(6): 1919e1926. 6. Zehetner J, DeMeester SR, Alicuben ET, et al. Intraoperative assessment of perfusion of the gastric graft and correlation with anastomotic leaks after esophagectomy. Ann Surg. 2015 Jul;262(1):74e78. 7. Campbell C, Reames MK, Robinson M, Symanowski J, Salo JC. Conduit vascular evaluation is associated with reduction in anastomotic leak after esophagectomy. J Gastrointest Surg. 2015 May;19(5):806e812. 8. Low DE, Alderson D, Cecconello I, et al. International consensus on standardization of data collection for complications associated with esophagectomy: esophagectomy complications consensus group (ECCG). Ann Surg. 2015 Aug;262(2):286e294. 9. Raymond DP, Seder CW, Wright CD, et al. Predictors of major morbidity or mortality after resection for esophageal cancer: a society of thoracic surgeons general thoracic surgery database risk adjustment model. Ann Thorac Surg. 2016 Jul;102(1):207e214. 10. Ryan CE, Paniccia A, Meguid RA, McCarter MD. Transthoracic anastomotic leak after esophagectomy: current trends. Ann Surg Oncol. 2017 Jan;24(1):281e290. 11. Alanezi K, Urschel JD. Mortality secondary to esophageal anastomotic leak. Ann Thorac Cardiovasc Surg. 2004 Apr;10(2):71e75. €genur I. Indocyanine green fluorescence angiog12. Degett TH, Andersen HS, Go raphy for intraoperative assessment of gastrointestinal anastomotic perfusion: a systematic review of clinical trials. Langenbecks Arch Surg. 2016 Sep;401(6): 767e775. 13. Nguyen NT, Hinojosa MW, Smith BR, Chang KJ, Gray J, Hoyt D. Minimally invasive esophagectomy: lessons learned from 104 operations. Ann Surg. 2008 Dec;248(6):1081e1091.
Please cite this article in press as: Dalton BGA, et al., Near infrared perfusion assessment of gastric conduit during minimally invasive Ivor Lewis esophagectomy, The American Journal of Surgery (2017), https://doi.org/10.1016/j.amjsurg.2017.11.026
Contents lists available at ScienceDirect
The American Journal of Surgery journal homepage: www.americanjournalofsurgery.com
Near infrared perfusion assessment of gastric conduit during minimally invasive Ivor Lewis esophagectomy Brian G.A. Dalton, Abubaker A. Ali, Marie Crandall, Ziad T. Awad* Department of Surgery, University of Florida Health- Jacksonville, United States
a r t i c l e i n f o
a b s t r a c t
Article history: Received 27 September 2017 Received in revised form 31 October 2017 Accepted 6 November 2017
Introduction: Anastomotic leak and conduit necrosis are devastating complications following Ivor Lewis esophagectomy. Near infrared imaging (NIR) using IndoCyanine Green allows for real time tissue perfusion assessment which may reduce anastomotic leak during minimally invasive Ivor Lewis esophagectomy (MIE). Methods: Forty consecutive MIE were performed by a single surgeon at a tertiary referral center. The first 20 were assessed for gastric conduit perfusion by clinical criteria (Group 1). The second 20 were also assessed using NIR laparoscopic system (Group 2). Results: Comparing Group 1 to Group 2, no significant differences were found in overall complication rate, readmission or reoperation rate. NIR resulted in resection of the non perfused proximal portion of the conduit in 30% (6/20). Two patients in group 2 group developed anastomotic leak (2/20) compared to 0 in Group 1 (p ¼ 0.49). Graft necrosis led to one mortality in Group 1, while there were 0 mortalities in Group 2. (p ¼ 1.0). Conclusion: Although NIR plays a role in assessment of tissue perfusion, in our study its use did not result in reduction of anastomotic leak rate. © 2017 Elsevier Inc. All rights reserved.
Keywords: Near infrared imaging Ivor Lewis esophagectomy Minimally invasive esophagectomy Indocyanine green angiography Anastomotic leak Graft necrosis
1. Introduction Esophagectomy is one of most invasive procedures in gastrointestinal surgery and despite improvements in surgical techniques and perioperative care, the mortality rate remains high.1 A study using the National Surgery Quality Improvement Program database (NSQIP) between 2006 and 2011 reported that the morbidity of patients with esophagectomy was 43.8% and mortality was 3.8%.2 In particular, anastomotic leak after esophagectomy remains an important cause of patient morbidity and impaired quality of life.3e5 In the majority of cases, reconstruction after esophagectomy is done using a gastric conduit that is perfused by the right gastroepiploic arcade. Perfusion at the proximal portion of the graft, in the area where the anastomosis is typically created, is variable but often tenuous because the gastroepiploic arcade rarely reaches the tip of the graft. Instead, the most proximal portion of the graft is typically perfused by intramural capillaries within the wall of the
* Corresponding author. Division of General and Gastrointestinal Surgery, University of Florida Health- Jacksonville, 653 West 8th Street, Jacksonville, FL 32209, United States. E-mail address: [email protected]fl.edu (Z.T. Awad).
stomach and small vessels in the omentum along the greater curvature.6 Historically, evaluation of the blood flow of the gastric conduit has been a challenge to most surgeons as relying on inspection of the color of gastric serosa is often inaccurate and misleading. Indocyanine green (ICG) fluorescence angiography and Doppler examination have recently been used to assess blood supply and assist in conduit construction. These modalities have been employed in an effort to reduce anastomotic complications after esophagectomy.6,7 The Near Infrared (NIR) laparoscopic system (PINPOINT Endoscopic Fluorescence Imaging System, NOVADAQ, Mississauga, ON, Canada) is used to provide high definition (HD) white light imaging during minimally invasive surgery (MIS), as well as NIR irradiation and ICG fluorescence emission imaging. This system provides a real-time false-color superimposition of ICG fluorescence signal on the HD white light view. This overlay allows simultaneous appreciation of dynamic perfusion and visualization of the conventional MIS video image. In theory, the PINPOINT system might provide valuable real-time information about perfusion of the gastric graft during minimally invasive Ivor Lewis esophagectomy (MIE) and this might influence
https://doi.org/10.1016/j.amjsurg.2017.11.026 0002-9610/© 2017 Elsevier Inc. All rights reserved.
Please cite this article in press as: Dalton BGA, et al., Near infrared perfusion assessment of gastric conduit during minimally invasive Ivor Lewis esophagectomy, The American Journal of Surgery (2017), https://doi.org/10.1016/j.amjsurg.2017.11.026
2
B.G.A. Dalton et al. / The American Journal of Surgery xxx (2017) 1e4
resection margins and surgical outcomes. The hypothesis is the use PINPOINT system during MIE esophagectomy would reduce anastomotic leak rates. 2. Methods After Institutional Review Board approval (IRB#201600651) a retrospective analysis of prospectively collected data of all MIE performed at our institution was performed. All MIE from April 2014 to January 2016 were included. All surgeries were performed for cancer and were performed by a single surgeon (ZA) at a tertiary referral center. Cases were analyzed in 2 groups. Group 1, the conduit was evaluated using standard clinical criteria by inspecting the color of the gastric serosa. Group 2, NIR technology was used intraoperatively for assessment of graft perfusion. Data is presented as mean ± standard deviation unless otherwise stated. Significance is defined as P 0.05. Comparative analysis was performed using student t test for continuous variables and Fishers exact for binary variables or Chi square test with Pearson correlation where appropriate.
Fig. 2. Gastric conduit after ICG injection on NIR with poor perfusion evident in proximal conduit. Line of perfusion demarcation (arrows) shown in PINPOINT modes.
3. Technique The abdominal portion of the procedure was performed laparoscopically. Dissection began by opening the gastrocolic omentum below the level of the pylorus, taking care to preserve the right gastroepiploic arcade. The right gastric artery was preserved in all patients. The greater curvature of the stomach was mobilized and the short gastric vessels are divided. The left gastric artery was dissected and transected using the vascular stapler after all nodal tissue is lifted off the celiac axis. A 5 cm wide gastric conduit (Fig. 1) was constructed using multiple firings of the laparoscopic linear stapler. Pyroloplasty was performed in all patients. The thoracic portion was performed thoracoscopically with the patient in the left lateral decubitus position. The inferior pulmonary ligament was incised and the right lung was retracted. The mediastinal pleura was incised and the esophagus was dissected to the level of the azygous vein, which was divided using the laparoscopic vascular stapler. The gastric conduit was pulled into the right chest, the specimen removed and end to end esophagogastric anastomosis was constructed intracorporeally using the mechanical circular stapler 25 mm DST XL EEA (Covidien, Newhaven, CT, USA). Beginning in February 2015, NIR assessment of conduit perfusion was done using the PINPOINT system - 7.5 mg of ICG is injected intravenously and conduit perfusion assessment is done 60 s after injection. A marking silk stitch was placed when there was a demarcation between the perfused and non-perfused part of the conduit (Fig. 2). The non-perfused segment was resected in the chest, and the anastomosis was constructed between the native esophagus and perfused proximal stomach.
Fig. 3. Gastric conduit after ICG injection showing good perfusion throughout conduit.
When the conduit appeared well perfused throughout (Fig. 3) a stitch was still placed on the anterior surface of the conduit for orientation purposes upon transposition into the chest. All patients underwent upper GI contrast study on day 4 prior to oral intake. Anastomotic leak was defined as full thickness defect of esophagus, conduit, anastomosis or staple line.8 Oral intake was started the day of upper GI contrast study if the study was negative for leak. 4. Results During the study period, 40 consecutive patients having undergone MIE. Group 1, 20 consecutive patients (April 2014eJanuary 2015). Group 2, 20 consecutive patients (February 2015eJanuary 2016) were NIR was used. The administration of ICG caused no adverse events in the NIR group. No differences were found between the 2 groups with regard demographic or preoperative parameters (Table 1).
Table 1 Demographic and preoperative date Group 1 vs Group 2.
Fig. 1. Tubularized gastric conduit.
Value
Group 1 (n ¼ 20)
Group 2 (n ¼ 20)
P value
Age (years) % Male BMI (kg/m2) % adenocarcinoma Neoadjuvant therapy (%) COPD (%) Coronary artery disease (%) Peroperative albumin (mg/dL)
66.2 ± 8 80 26.3 ± 4.1 70 95 20 15 3.9 ± 0.4
61.8 ± 12.8 80 26.4 ± 4.9 90 85 15 25 3.9 ± 0.4
0.2 1 0.97 0.24 0.6 1 0.69 0.69
COPD: chronic obstructive pulmonary disease.
Please cite this article in press as: Dalton BGA, et al., Near infrared perfusion assessment of gastric conduit during minimally invasive Ivor Lewis esophagectomy, The American Journal of Surgery (2017), https://doi.org/10.1016/j.amjsurg.2017.11.026
B.G.A. Dalton et al. / The American Journal of Surgery xxx (2017) 1e4 Table 2 Perioperative outcomes Group 1 and Group 2. Value
Group 1 (n ¼ 20)
Group 2 (n ¼ 20)
P value
Anastomotic leak (%) Graft necrosis (%) Length of stay (days) Overall complication rate (%) Reoperation within same admission (%) 90 day reoperation (%) 90 day readmission (%) 90 day mortality (%) Atrial fibrillation (%) Respiratory failure
0 5 8.1 ± 1.9 55 5
10 0 9.8 ± 4 40 10
0.49 1 0.09 0.53 1
15 20 5 25 10
15 10 0 25 0
1 0.66 1 1 0.49
All patients were diagnosed with esophageal cancer. There was no difference in operative time (371 ± 90 vs 379 ± 66 min, p ¼ 0.76) or estimated blood loss (159 ± 150 ml vs 338 ± 723, p ¼ 0.28) between the 2 groups. Mean blood loss and standard deviation (SD) in Group 2 was increased by the presence of one outlier (>2 SD outside the mean). This patient had an injury to an aberrant pulmonary vein branch which was controlled but the esophagogastrostomy was delayed until an operating room return 2 days later. This was also the only patient in the series to receive an intraoperative transfusion. No statistically significant differences were found between the 2 groups in overall complication rate, anastomotic leak, graft necrosis, reoperation or length of stay (Table 2). The use of NIR resulted in resection of proximal non-perfused proximal part of the conduit in 30% (6/20) of patients. The 2 leaks in the NIR were in the group that needed proximal conduit resection, and both leaks were managed with endoscopic stent placement. These endoscopic stents were placed in an elective fashion. In Group 1, 3 patients required surgical intervention within 90 days: one patient for wound infection required debridement at the jejunostomy site, one for cecal volvulus necessitating right colon resection, and the third patient was explored for graft necrosis. This patient underwent resection of the graft with cervical esophagostomy, and was the only mortality from either group. In Group 2, reoperation within 90 days were observed in 3 patients: one patient with conduit obstruction as a result of redundant conduit above the diaphragm, the patient with pulmonary vein branch injury described earlier, and one patient with post esophagectomy hiatal hernia. Ten total patients were diagnosed with postoperative atrial fibrillation. One of these patients required cardioversion (Group 2). One patient in the Group 1 was diagnosed with a Clostridium Difficile infection and was treated with antibiotics. Another patient in Group 1 developed colonic pseudo-obstruction and was treated non-operatively. 5. Discussion A large database study examining all modalities of esophagectomy showed overall major morbidity of esophagectomy to be 33.8% and anastomotic leak rate of 12.9%.9 Anastomotic leak has also been linked to increased morbidity in patients undergoing esophagectomy.10,11 Our study did not answer the question if NIR can reduce the anastomotic leak rate. Zehetner et al. using SPY Imaging System (Novadaq, Ontario, Canada) among patients undergoing open transhiatal esophagectomy showed a significantly higher leak rate (45% vs 2%, p < 0.0001) when the anastomosis was performed to an area of gastric conduit distal to the line of perfusion demarcation.6 Campbell et al. employed both Doppler and intraoperative ICG
3
fluorescence angiography- SPY Elite System (LifeCell, Bridgewater, NJ, USA) among patients undergoing Ivor Lewis esophagectomy.7 They adopted a quantitative perfusion cutoff of 75% as the area where the esophagogastric anastomosis was performed, usually 10 cm above the pylorus. The leak rate was 0% (30 patients) when the anastomosis was placed proximal to the 75% relative perfusion line compared to 20% leak rate (60 patients) prior to the use of either technology.7 In both studies,6,7 a midline abdominal incision is required to deliver the conduit to the outside for quantitative perfusion assessment using SPY System or intraoperative Doppler, while our approach is pure minimally invasive (laparoscopic and thoracoscopic). We did not use laparoscopic Doppler and relied solely on qualitative assessment of gastric conduit perfusion. If quantitative data were available with the PINPOINT system establishing a standardized level of perfusion necessary for successful anastomosis, this could play a role in reducing anastomotic leak rate. Degett et al. in a systemic literature review of ICG- FA (fluorescence angiography) to assess perfusion during construction of a primary gastrointestinal anastomosis showed the technique to be associated with reduced risk of anastomotic colorectal leaks compared with no ICG-FA.12 However, the anastomotic leakage rate in patients with esophageal anastomoses and intraoperative ICG-FA assessment was 14% (n ¼ 30/214). None of the studies involving esophageal anastomoses had a control group without ICG-FA assessment. They concluded that ICG-FA is a feasible and promising tool. However, heterogeneous studies and the lack of high level of evidence the clinical benefit of ICG-FA is inconclusive. Furthermore, the technique remains subjective until more objective cutoff levels for sufficient perfusion has been established.12 In our study, 6/20 (30%) of patients underwent resection of non-perfused proximal gastric conduit using the NIR, allowing a well-perfused gastric conduit to be consistently used for the esophagogastric anastomosis. It is concerning, however, that anastomotic leaks were observed in 2/6 (33.33%) patients in this group, and raises the possibility that proximal resection might have created undue anastomotic tension and compromised blood supply. Although tension is difficult to assess and quantify, especially when minimally invasive surgery is utilized, we routinely roll the anastomosis from side to side and lift it to examine the entire staple line; this maneuver would not be possible had the anastomosis being under tension. Is it unknown whether those patients with demarcation between the perfused and non-perfused part of the conduit using NIR are at risk of anastomotic failure, and proximal resection was a marker of a potentially higher-risk anastomosis. Other authors agree with our opinion that the intra-thoracic anastomosis provides the ability to resect the tip of the gastric conduit, and the anastomosis is not under excessive tension13 as the surgeon has control on the level of transection of the esophagus relative to the location of the esophageal cancer. Limitations of this study include small population, retrospective nature, single center and single surgeon, all of which introduce potential bias. However, to our knowledge, the present study is the first using the PINPOINT system for graft perfusion assessment among patients undergoing strict laparoscopic/thoracoscopic esophagectomy. Future directions of research include studying this modality of NIR using quantified perfusion values should they come available. We would hope to establish a level of perfusion that results in a negligible anastomotic leak rate. 6. Conclusion In our study, the use of NIR or interventions based on its findings did not result in reduction of anastomotic leak rate. Better quantitative integrated metrics are needed to better define tissue
Please cite this article in press as: Dalton BGA, et al., Near infrared perfusion assessment of gastric conduit during minimally invasive Ivor Lewis esophagectomy, The American Journal of Surgery (2017), https://doi.org/10.1016/j.amjsurg.2017.11.026
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B.G.A. Dalton et al. / The American Journal of Surgery xxx (2017) 1e4
perfusion using the PINPOINT system. Further studies are warranted to validate the use of this novel technology. Conflicts of interest No conflicts of interest were encountered during this project by any of the authors. No external financial or material support was provided, and there are no commercial or financial interests related to the topic. Author contributions BD: Data collection, analysis, interpretation, manuscript drafting, critical revision AA: Study design, data collection, critical revision. MC: Interpretation, manuscript drafting, critical revision. ZA: Study design, data collection, analysis, interpretation, manuscript drafting, critical revision. All authors agree to the manuscript its submitted form and attest to the accuracy of the data and interpretation of the data. References 1. Saeki H, Masuda T, Okada S, et al. Impact of perioperative peripheral blood values on postoperative complications after esophageal surgery. Surg Today. 2010 Jul;40(7):626e631. 2. Lucas DJ, Pawlik TM. Quality improvement in gastrointestinal surgical oncology with American college of surgeons national surgical quality improvement Program. Surgery. 2014 Apr;155(4):593e601.
3. Fernandez FG, Meyers BF. Quality of life after esophagectomy. Semin Thorac Cardiovasc Surg. 2004;16(2):152e159. Summer. 4. Schuchert MJ, Abbas G, Nason KS, et al. Impact of anastomotic leak on outcomes after transhiatal esophagectomy. Surgery. 2010 Oct;148(4):831e838. discussion 838e840. 5. Kassis ES, Kosinski AS, Ross Jr P, Koppes KE, Donahue JM, Daniel VC. Predictors of anastomotic leak after esophagectomy: an analysis of the society of thoracic surgeons general thoracic database. Ann Thorac Surg. 2013 Dec;96(6): 1919e1926. 6. Zehetner J, DeMeester SR, Alicuben ET, et al. Intraoperative assessment of perfusion of the gastric graft and correlation with anastomotic leaks after esophagectomy. Ann Surg. 2015 Jul;262(1):74e78. 7. Campbell C, Reames MK, Robinson M, Symanowski J, Salo JC. Conduit vascular evaluation is associated with reduction in anastomotic leak after esophagectomy. J Gastrointest Surg. 2015 May;19(5):806e812. 8. Low DE, Alderson D, Cecconello I, et al. International consensus on standardization of data collection for complications associated with esophagectomy: esophagectomy complications consensus group (ECCG). Ann Surg. 2015 Aug;262(2):286e294. 9. Raymond DP, Seder CW, Wright CD, et al. Predictors of major morbidity or mortality after resection for esophageal cancer: a society of thoracic surgeons general thoracic surgery database risk adjustment model. Ann Thorac Surg. 2016 Jul;102(1):207e214. 10. Ryan CE, Paniccia A, Meguid RA, McCarter MD. Transthoracic anastomotic leak after esophagectomy: current trends. Ann Surg Oncol. 2017 Jan;24(1):281e290. 11. Alanezi K, Urschel JD. Mortality secondary to esophageal anastomotic leak. Ann Thorac Cardiovasc Surg. 2004 Apr;10(2):71e75. €genur I. Indocyanine green fluorescence angiog12. Degett TH, Andersen HS, Go raphy for intraoperative assessment of gastrointestinal anastomotic perfusion: a systematic review of clinical trials. Langenbecks Arch Surg. 2016 Sep;401(6): 767e775. 13. Nguyen NT, Hinojosa MW, Smith BR, Chang KJ, Gray J, Hoyt D. Minimally invasive esophagectomy: lessons learned from 104 operations. Ann Surg. 2008 Dec;248(6):1081e1091.
Please cite this article in press as: Dalton BGA, et al., Near infrared perfusion assessment of gastric conduit during minimally invasive Ivor Lewis esophagectomy, The American Journal of Surgery (2017), https://doi.org/10.1016/j.amjsurg.2017.11.026