CC BY 4.0 · European J Pediatr Surg Rep. 2023; 11(01): e32-e35
DOI: 10.1055/s-0043-1769106
Case Report

Hyperspectral Imaging—A Novel Tool to Assess Tissue Perfusion and Oxygenation in Esophageal Anastomoses

Duarte Vaz Pimentel
1   Department of Pediatric Surgery, University Hospital Leipzig, Leipzig, Sachsen, Germany
,
Larissa Merten
1   Department of Pediatric Surgery, University Hospital Leipzig, Leipzig, Sachsen, Germany
,
Jan-Hendrik Gosemann
1   Department of Pediatric Surgery, University Hospital Leipzig, Leipzig, Sachsen, Germany
,
Ines Gockel
2   Department of Visceral, Transplantation, Thoracic and Vascular Surgery, University Hospital Leipzig, Leipzig, Sachsen, Germany
,
Boris Jansen-Winkeln
2   Department of Visceral, Transplantation, Thoracic and Vascular Surgery, University Hospital Leipzig, Leipzig, Sachsen, Germany
,
Steffi Mayer
1   Department of Pediatric Surgery, University Hospital Leipzig, Leipzig, Sachsen, Germany
,
Martin Lacher
1   Department of Pediatric Surgery, University Hospital Leipzig, Leipzig, Sachsen, Germany
› Author Affiliations
 

Abstract

Anastomotic stricture and leakage are common complications after repair of esophageal atresia (EA). A compromised perfusion of the anastomosis is a contributing factor. Hyperspectral imaging (HSI) is an ultrashort noninvasive method to measure tissue perfusion. We present two cases of with tracheoesophageal fistula (TEF)/EA repair, in whom we applied HSI: the first patient was a newborn with EA type C who underwent open TEF repair. The second one had an EA type A and cervical esophagostomy, in whom we performed gastric transposition. In both patients, HSI confirmed a good tissue perfusion of the later anastomosis. The postoperative course was uneventful and both patients are on full enteral feeds. We conclude that HSI is a safe and noninvasive tool that allows near real-time assessment of tissue perfusion and can contribute to the identification of the optimal anastomotic region during pediatric esophageal surgery.


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New Insights and the Importance for a Pediatric Surgeon

We describe the first use of HSI (a safe and noninvasive tool that allows near real-time assessment of tissue perfusion and can contribute to the identification of the optimal anastomotic region) in pediatric esophageal surgery.

Introduction

Esophageal atresia (EA) with or without tracheoesophageal fistula (TEF) has an incidence of 1 in 4,099 births.[1] Anastomotic stricture and leakage are frequent problems following repair of EA/TEF, often due to tension on or compromised perfusion of the anastomosis.[2] [3] Anastomotic strictures require 5.1 ± 5.6 dilatations on average. Almost all patients require at least one readmission within the first year of life.[4] The intraoperative assessment of tissue perfusion has recently gained increasing interest in gastrointestinal surgery.[5] Different methods have been established, the most prevalent being indocyanine green fluorescence scan.[6] [7] A drawback of this and other techniques to assess tissue perfusion is the need to inject contrast agents with potential adverse reactions and toxicity.[8]

Hyperspectral imaging (HSI) is a noninvasive tool for the assessment of tissue perfusion and oxygenation based on the tissue-specific reflection of light in hyperspectral ranges of visible and near-infrared light (500–1,000 nm wavelength).[9] It does not require contrast agents and provides near real-time information on tissue perfusion (near-infrared perfusion index [NIR-PI]), tissue hemoglobin index (THI), and tissue oxygen saturation (StO2) with 10 to 15 seconds delay.

HSI has been applied to various fields of surgery including cutaneous flaps in reconstructive surgery, partial nephrectomies, or intestinal anastomoses.[10] [11] [12] [13] We report the first application of HSI in pediatric esophageal surgery.


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Case Description

Case 1: A newborn girl (body weight 1,850 g, gestational age 36 weeks) presented with VACTERL association including EA type C, anorectal malformation with vestibular fistula, and septum defect. She underwent open TEF repair on day 2 of life. After TEF closure, the tip of the lower esophagus showed an impaired perfusion on real-time HSI assessment (NIR-PI 58%; THI 100%; StO2 40%; [Fig. 1A, B]). Thus, an additional 2 mm of the lower esophagus ([Fig. 2]) were resected to accomplish an anastomosis in a well-perfused area (NIR-PI 92%; THI 100%; StO2 55%; [Fig. 1C, D]). The postoperative course was uneventful. No anastomotic leak or stenosis occurred. The patient was discharged home on postoperative day 41 due to difficulties related to her low birth weight and cardiac situation. During the further course of 22 months, no esophageal dilatations were required.

Zoom Image
Fig. 1 Intraoperative situs (A, C) and HSI StO2 (B, D) after TEF ligation: Well-perfused upper esophageal pouch (o) and impaired perfusion of the lower esophagus (#) before resection of its distal tip (A, B). After resection of the tip of the distal pouch (Fig. 2), improved perfusion with only minor impairment at the anastomotic suture line itself (arrow) was detected (C, D). HSI, hyperspectral imaging; StO2, tissue oxygen saturation; TEF, tracheoesophageal fistula.
Zoom Image
Fig. 2 Additional resection of 2 mm distal esophagus after hyperspectral imaging measurement.

Case 2: A 9-month-old boy with EA type A underwent gastric transposition after receiving a cervical esophagostomy in the newborn period at another institution. After laparotomy, a good perfusion of the gastric fundus was confirmed and a cervical esophagogastric anastomosis was established (StO2 80%, THI 100%, NIR-PI 80%; [Fig. 3]). The subsequent course remained uneventful for 26 months. No dilation of the cervical anastomosis was required. The patient is on full oral feeds.

Zoom Image
Fig. 3 Intraoperative situs (A) and HSI assessment (StO2 [B], THI [C], and NIR-PI [D]) before esophagogastric anastomosis for gastric transposition. o, fundus; *, greater curvature; #, antrum; HSI, hyperspectral imaging; NIR-PI, near-infrared perfusion index; StO2, tissue oxygen saturation; THI, tissue hemoglobin index.

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Discussion

Anastomotic leakage and stricture after repair of EA/TEF occur in ∼20 and 28% of cases, respectively.[14] This is, among other factors, caused by an impaired perfusion of the anastomosis.[15] Although intraoperatively the perfusion of the lower esophagus appeared unaltered macroscopically in patient 1, HSI measurement revealed a diminished perfusion of the distal pouch. Thus, HSI had an additional diagnostic value. We therefore resected additional 2 mm of the distal esophagus to create an anastomosis of the two esophageal ends, which were well perfused. Of note, we recognized an impaired perfusion at the anastomosis itself, most likely from the suture line ([Fig. 1]), which has been described in adults before.[11]

Currently, several clinical studies are ongoing to evaluate the benefits of HSI in gastrointestinal anastomoses. A more peripheral adaptation of the anastomosis based on intraoperative HSI was reported for oncologic esophagectomy in 38% of patients without any postoperative leak.[16] In another study reporting on colorectal resection, a deviation between the transection line planned by the surgeon and the border line visualized by HSI of 1 to 13 mm was found for all patients. Consequently, the resection area was corrected proximally in 21% of patients due to the intraoperative HSI records. Thus, the authors concluded that the determination of the resection margin by HSI provide the surgeon with an objective decision aid for assessment of the best possible perfusion and ideal anastomotic area in colorectal surgery.[17] Its transferability to other gastrointestinal anastomoses is obvious. However, normal or cutoff values for different gastrointestinal anastomotic types especially in pediatric surgery are still required.

Besides HSI, other methods such as indocyanine green fluorescence can also assess intraoperative perfusion and guide surgeons to improve surgical outcomes.[18] However, this technique requires contrast agents, which is not the case in HSI. HSI is a safe, fast, noninvasive technique that can easily be implemented during surgery. The tissue perfusion assessed by HSI is also comparable to that of indocyanine green fluorescence, which has recently been shown for colorectal resections as well as oncologic esophagectomy.[16] [19] HSI has also been shown to discriminate tissue perfusion in acute mesenteric ischemia and depict tissue viability via reflectance spectra.[20] Besides, it has been applied to evaluate liver and gastric perfusion during pancreatoduodenectomy and identifying exact resection planes for anatomic liver resection.[21] [22]

Only recently, also, a HSI system for minimally invasive surgery has been introduced. The HSI laparoscope available has a diameter of 10 mm and is consistent for object distances up to 10 cm.[23] [24] It is currently examined for clinical practicability and impact in adult surgery.

These emerging experiences in adult surgery indicate promising applications in pediatric surgery. Future tasks include the implementation of HSI measurements in surgical interventions where adequate tissue perfusion plays a key role. However, to date, there are no reliable normal and cutoff measurements for decision-making. Moreover, prospective studies comparing intraoperative perfusion with postoperative outcomes are also lacking. However, we think that the HSI technique is easy to perform and a promising tool to assess perfusion in pediatric surgery, which may contribute to better in children.


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Conclusion

This is the first report on HSI assessment in pediatric surgery as a safe and noninvasive tool to assess tissue perfusion in real time. It can help determine the optimal anastomotic region during pediatric esophageal surgery.


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Conflict of Interest

None declared.

  • References

  • 1 Nassar N, Leoncini E, Amar E. et al. Prevalence of esophageal atresia among 18 international birth defects surveillance programs. Birth Defects Res A Clin Mol Teratol 2012; 94 (11) 893-899
  • 2 Askarpour S, Peyvasteh M, Javaherizadeh H, Askari N. Evaluation of risk factors affecting anastomotic leakage after repair of esophageal atresia. Arq Bras Cir Dig 2015; 28 (03) 161-162
  • 3 Touloukian RJ, Seashore JH. Thirty-five-year institutional experience with end-to-side repair for esophageal atresia. Arch Surg 2004; 139 (04) 371-374 , discussion 374
  • 4 Dingemann C, Dietrich J, Zeidler J. et al. Early complications after esophageal atresia repair: analysis of a German health insurance database covering a population of 8 million. Dis Esophagus 2016; 29 (07) 780-786
  • 5 Urbanavičius L, Pattyn P, de Putte DV, Venskutonis D. How to assess intestinal viability during surgery: a review of techniques. World J Gastrointest Surg 2011; 3 (05) 59-69
  • 6 Alander JT, Kaartinen I, Laakso A. et al. A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging 2012; 2012: 940585
  • 7 Turner SR, Molena DR. The role of intraoperative fluorescence imaging during esophagectomy. Thorac Surg Clin 2018; 28 (04) 567-571
  • 8 Alford R, Simpson HM, Duberman J. et al. Toxicity of organic fluorophores used in molecular imaging: literature review. Mol Imaging 2009; 8 (06) 341-354
  • 9 Lu G, Fei B. Medical hyperspectral imaging: a review. J Biomed Opt 2014; 19 (01) 10901
  • 10 Akbari H, Kosugi Y, Kojima K, Tanaka N. Hyperspectral imaging and diagnosis of intestinal ischemia. Annu Int Conf IEEE Eng Med Biol Soc 2008; 2008: 1238-1241
  • 11 Jansen-Winkeln B, Maktabi M, Takoh JP. et al. Hyperspektral-Imaging bei gastrointestinalen Anastomosen. Chirurg 2018; 89 (09) 717-725
  • 12 Best SL, Thapa A, Jackson N. et al. Renal oxygenation measurement during partial nephrectomy using hyperspectral imaging may predict acute postoperative renal function. J Endourol 2013; 27 (08) 1037-1040
  • 13 Gockel I, Jansen-Winkeln B, Holfert N. et al. Möglichkeiten und Perspektiven der Hyperspektralbildgebung in der Viszeralchirurgie. Chirurg 2020; 91 (02) 150-159
  • 14 Du J, Huang J, Li Y, Chen Y, Guo W, Hou D. The repair of esophageal atresia and major complications—a systematic review and our experience in dealing with the tracheoesophageal fistula. Ann Laparosc Endosc Surg 2019; 4: 90-90
  • 15 Mayer S, Gitter H, Göbel P. et al. Behandlung der Ösophagusatresie mit unterer tracheoösophagealer Fistel – Zusammenfassung der aktuellen S2K-Leitlinie der DGKCH. Klin Padiatr 2020; 232 (04) 178-186
  • 16 Hennig S, Jansen-Winkeln B, Köhler H. et al. Novel intraoperative imaging of gastric tube perfusion during oncologic esophagectomy-a pilot study comparing hyperspectral imaging (HSI) and fluorescence imaging (FI) with indocyanine green (ICG). Cancers (Basel) 2021; 14 (01) 97
  • 17 Jansen-Winkeln B, Holfert N, Köhler H. et al. Determination of the transection margin during colorectal resection with hyperspectral imaging (HSI). Int J Colorectal Dis 2019; 34 (04) 731-739
  • 18 Lau CT, Au DM, Wong KKY. Application of indocyanine green in pediatric surgery. Pediatr Surg Int 2019; 35 (10) 1035-1041
  • 19 Jansen-Winkeln B, Germann I, Köhler H. et al. Comparison of hyperspectral imaging and fluorescence angiography for the determination of the transection margin in colorectal resections-a comparative study. Int J Colorectal Dis 2021; 36 (02) 283-291
  • 20 Mehdorn M, Köhler H, Rabe SM. et al. Hyperspectral imaging (HSI) in acute mesenteric ischemia to detect intestinal perfusion deficits. J Surg Res 2020; 254: 7-15
  • 21 Moulla Y, Buchloh DC, Köhler H. et al. Hyperspectral imaging (HSI)-a new tool to estimate the perfusion of upper abdominal organs during pancreatoduodenectomy. Cancers (Basel) 2021; 13 (11) 2846
  • 22 Sucher R, Athanasios A, Köhler H. et al. Hyperspectral imaging (HSI) in anatomic left liver resection. Int J Surg Case Rep 2019; 62: 108-111
  • 23 Pfahl A, Köhler H, Thomaßen MT. et al. Video: clinical evaluation of a laparoscopic hyperspectral imaging system. Surg Endosc 2022; 36 (10) 7794-7799
  • 24 Köhler H, Kulcke A, Maktabi M. et al. Laparoscopic system for simultaneous high-resolution video and rapid hyperspectral imaging in the visible and near-infrared spectral range. J Biomed Opt 2020; 25 (08) 086004

Address for correspondence

Duarte Vaz Pimentel, MD
Department of Pediatric Surgery, Universitatsklinikum Leipzig
Liebigstr. 20a, Leipzig 04103
Germany   

Publication History

Received: 18 July 2021

Accepted: 03 October 2022

Article published online:
12 June 2023

© 2023. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

  • References

  • 1 Nassar N, Leoncini E, Amar E. et al. Prevalence of esophageal atresia among 18 international birth defects surveillance programs. Birth Defects Res A Clin Mol Teratol 2012; 94 (11) 893-899
  • 2 Askarpour S, Peyvasteh M, Javaherizadeh H, Askari N. Evaluation of risk factors affecting anastomotic leakage after repair of esophageal atresia. Arq Bras Cir Dig 2015; 28 (03) 161-162
  • 3 Touloukian RJ, Seashore JH. Thirty-five-year institutional experience with end-to-side repair for esophageal atresia. Arch Surg 2004; 139 (04) 371-374 , discussion 374
  • 4 Dingemann C, Dietrich J, Zeidler J. et al. Early complications after esophageal atresia repair: analysis of a German health insurance database covering a population of 8 million. Dis Esophagus 2016; 29 (07) 780-786
  • 5 Urbanavičius L, Pattyn P, de Putte DV, Venskutonis D. How to assess intestinal viability during surgery: a review of techniques. World J Gastrointest Surg 2011; 3 (05) 59-69
  • 6 Alander JT, Kaartinen I, Laakso A. et al. A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging 2012; 2012: 940585
  • 7 Turner SR, Molena DR. The role of intraoperative fluorescence imaging during esophagectomy. Thorac Surg Clin 2018; 28 (04) 567-571
  • 8 Alford R, Simpson HM, Duberman J. et al. Toxicity of organic fluorophores used in molecular imaging: literature review. Mol Imaging 2009; 8 (06) 341-354
  • 9 Lu G, Fei B. Medical hyperspectral imaging: a review. J Biomed Opt 2014; 19 (01) 10901
  • 10 Akbari H, Kosugi Y, Kojima K, Tanaka N. Hyperspectral imaging and diagnosis of intestinal ischemia. Annu Int Conf IEEE Eng Med Biol Soc 2008; 2008: 1238-1241
  • 11 Jansen-Winkeln B, Maktabi M, Takoh JP. et al. Hyperspektral-Imaging bei gastrointestinalen Anastomosen. Chirurg 2018; 89 (09) 717-725
  • 12 Best SL, Thapa A, Jackson N. et al. Renal oxygenation measurement during partial nephrectomy using hyperspectral imaging may predict acute postoperative renal function. J Endourol 2013; 27 (08) 1037-1040
  • 13 Gockel I, Jansen-Winkeln B, Holfert N. et al. Möglichkeiten und Perspektiven der Hyperspektralbildgebung in der Viszeralchirurgie. Chirurg 2020; 91 (02) 150-159
  • 14 Du J, Huang J, Li Y, Chen Y, Guo W, Hou D. The repair of esophageal atresia and major complications—a systematic review and our experience in dealing with the tracheoesophageal fistula. Ann Laparosc Endosc Surg 2019; 4: 90-90
  • 15 Mayer S, Gitter H, Göbel P. et al. Behandlung der Ösophagusatresie mit unterer tracheoösophagealer Fistel – Zusammenfassung der aktuellen S2K-Leitlinie der DGKCH. Klin Padiatr 2020; 232 (04) 178-186
  • 16 Hennig S, Jansen-Winkeln B, Köhler H. et al. Novel intraoperative imaging of gastric tube perfusion during oncologic esophagectomy-a pilot study comparing hyperspectral imaging (HSI) and fluorescence imaging (FI) with indocyanine green (ICG). Cancers (Basel) 2021; 14 (01) 97
  • 17 Jansen-Winkeln B, Holfert N, Köhler H. et al. Determination of the transection margin during colorectal resection with hyperspectral imaging (HSI). Int J Colorectal Dis 2019; 34 (04) 731-739
  • 18 Lau CT, Au DM, Wong KKY. Application of indocyanine green in pediatric surgery. Pediatr Surg Int 2019; 35 (10) 1035-1041
  • 19 Jansen-Winkeln B, Germann I, Köhler H. et al. Comparison of hyperspectral imaging and fluorescence angiography for the determination of the transection margin in colorectal resections-a comparative study. Int J Colorectal Dis 2021; 36 (02) 283-291
  • 20 Mehdorn M, Köhler H, Rabe SM. et al. Hyperspectral imaging (HSI) in acute mesenteric ischemia to detect intestinal perfusion deficits. J Surg Res 2020; 254: 7-15
  • 21 Moulla Y, Buchloh DC, Köhler H. et al. Hyperspectral imaging (HSI)-a new tool to estimate the perfusion of upper abdominal organs during pancreatoduodenectomy. Cancers (Basel) 2021; 13 (11) 2846
  • 22 Sucher R, Athanasios A, Köhler H. et al. Hyperspectral imaging (HSI) in anatomic left liver resection. Int J Surg Case Rep 2019; 62: 108-111
  • 23 Pfahl A, Köhler H, Thomaßen MT. et al. Video: clinical evaluation of a laparoscopic hyperspectral imaging system. Surg Endosc 2022; 36 (10) 7794-7799
  • 24 Köhler H, Kulcke A, Maktabi M. et al. Laparoscopic system for simultaneous high-resolution video and rapid hyperspectral imaging in the visible and near-infrared spectral range. J Biomed Opt 2020; 25 (08) 086004

Zoom Image
Fig. 1 Intraoperative situs (A, C) and HSI StO2 (B, D) after TEF ligation: Well-perfused upper esophageal pouch (o) and impaired perfusion of the lower esophagus (#) before resection of its distal tip (A, B). After resection of the tip of the distal pouch (Fig. 2), improved perfusion with only minor impairment at the anastomotic suture line itself (arrow) was detected (C, D). HSI, hyperspectral imaging; StO2, tissue oxygen saturation; TEF, tracheoesophageal fistula.
Zoom Image
Fig. 2 Additional resection of 2 mm distal esophagus after hyperspectral imaging measurement.
Zoom Image
Fig. 3 Intraoperative situs (A) and HSI assessment (StO2 [B], THI [C], and NIR-PI [D]) before esophagogastric anastomosis for gastric transposition. o, fundus; *, greater curvature; #, antrum; HSI, hyperspectral imaging; NIR-PI, near-infrared perfusion index; StO2, tissue oxygen saturation; THI, tissue hemoglobin index.