The use of fluorescence angiography to assess bowel viability in the acute setting: an international, multi-centre case series

We performed a retrospective analysis of a non-consecutive case series of all patients undergoing emergency surgery for bowel ischaemia in which FA was performed between February 2016 and 2021 in three tertiary referral centres. This study has been approved by the medical ethical committee of the Amsterdam University Medical Centres (AUMC)—location Amsterdam Medical Centre and has therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. This case series has been reported in line with the PROCESS Guideline [12]. Inclusion criteria were patients over 18 years old that underwent FA using indocyanine green (ICG) to assess intestinal perfusion during an emergency procedure for suspicion of bowel ischaemia. Patients were excluded when FA was performed after intestinal resection or with the sole purpose to assess perfusion of an anastomosis. Patient data with baseline characteristics, operative details and postoperative outcomes were retrospectively collected from the prospective maintained electronic patient systems of the different hospitals.

This international, multi-centre cohort study describes the use and outcomes of FA in the acute setting. Although FA has been widely implemented in the clinical setting for elective surgery, the potential added value in the acute setting has barely been studied. Among 93 operations for acute bowel ischaemia, a change of management was observed in 29%, resulting in bowel preservation in approximately one out of four patients without a substantial increase in unplanned reoperations. The overall reoperation rate was 12% and the 30-day mortality was 18%, both of which are low compared to other published series [1‐4, 13]. In half of the patients that underwent bowel resection, a primary anastomosis was made. In these patients, an acceptable leak rate of 4% was found.

This study also emphasizes that a median of 50 cm (IQR 28–98) of bowel could be spared among patients with a CoM-FA with a more conservative approach. Preserving 50 cm of small bowel or colon could make the difference in patients with extensive resections in preventing subsequent short bowel syndrome (which tends to occur when less of 100 cm of functioning bowel remains) [14].

The number of CoM-FA reported in this study corresponds with two prior studies investigating the use of FA in the acute setting; in both studies, FA provided additional information in 32–34.6% of the cases [15, 16]. While definitive randomized control trials are currently ongoing [17], existing literature indicates that ICG use in vascularization assessment impacts the user’s decision making in the elective setting in approximately 5–15% of cases [18, 19]. It seems therefore that FA assessments alter the surgical strategy more often in the acute than in the elective setting.

In our study, there was an overall reoperation rate of 12%. This was 29% in patients in whom the CoM- FA encouraged preservation of bowel versus 8% in those in whom there was no CoM-FA. It’s concerning that three patients in this group had further ischaemia identified and the mortality of this group was also higher than those in whom either no change or a more aggressive approach was followed. Some of the increased reoperation rate may be due to surgeons planning a second look with a lower threshold or to perform a delayed anastomosis after a more conservative approach is conceivable. Unplanned operation rates were similar between those without CoM-FA (7%) as with those in whom CoM-FA preserved bowel (10%) and in both groups, one patient was found to have progressive ischaemia. Three of the four cases requiring additional resection, however, took place in the conservative group, indicating that FA interpretation could be misleading and might require a proper learning curve to be proficient. As acute surgery is often performed out of office hours, the surgeon on call might have less experience using FA and interpret the FA differently than a more experienced user would, it has recently been demonstrated that there is a significant inter-observer variability of the interpretation of fluorescence imaging between expert and non-expert users in the elective setting [20]. Besides, in the acute setting, the surgeon has to contend with haemodynamic unstable patients with vasopressor requirement, which might result in difficult to interpret fluorescence images. When preserving bowel due to FA, there does seem to be a higher risk of progressive ischaemia and performing a planned reoperation (second look) at a lower threshold should be considered when preserving bowel.

The overall 30-day mortality was 18% (n = 17/93) in this series. If one looks at the mortality rates within the CoM-FA groups (Table 2), there is a higher mortality rate (24% in conservative group and 33% in the more aggressive approach group), compared to the no CoM-FA group (15%). This is noteworthy; however, this does not necessarily mean that this is related to the change of management itself. The CoM-FA groups have a different aetiology than the no change group, i.e. a higher proportion of mesenteric ischaemia, which is associated with a higher morbidity and mortality [3, 4]. Besides, in the CoM-FA group, there was a higher proportion of patients with an ASA score of IV; 44% versus 21% (Table 1). Also, it may be those who had CoM-FA had more complex ischaemic patterns to judge while those without were more discrete. It's noteworthy that consultant-case had higher mortality overall then those done by more junior staff, similarly suggesting differences other than this parameter alone.

While FA seems associated with positive outcomes in the overall group, the concerns identified in this study accentuate the need for further careful research including perhaps data-banking of the videos to allow understanding of the perfusion appearances and user interpretations. For instance, after reviewing FA images of patients who had progressive ischaemia during reoperation, two videos gave the impression of diffusion rather than adequate perfusion in the more conservative group and in our opinion should have been resected initially. This would also allow for training of surgeons without each having to acquire individual expert experience on the job. Furthermore quantification methods, with quantitative values that define a threshold for adequate perfusion, may help standardize interpretations. In addition, protocolized approaches are needed to be developed. From our own experience, endorsed by this study, we suggest that perfusion judgement should be determined within the first minute as, even though the bowel may fluoresce later, this may be falsely positive occurring due to diffusion of ICG into the tissue rather than true perfusion [21].

This study was limited by its retrospective nature. However, CoM-FA was reported in the operation reports prospectively. Yet, due to the retrospective nature of this study, we could not distinguish between the different kinds of aetiology of non-adhesional and non-volvulus bowel ischaemia (i.e. whether low flow, thrombotic disease, non-occlusive mesenteric ischaemia). In addition, quantitative values such as time to fluorescence were not captured. Besides, patients were not consecutively included, which may have resulted in a selection bias. There is also a lack of contemporaneous control data to give context to the clinical outcomes here reported. Prospective studies which both include quantitative fluorescence values as well as differentiate between the different manifestations of intestinal ischaemia are needed.

In conclusion, this study, the largest multi-centre case series yet, presents the use of FA in the acute setting of patients operated on because of ischaemia. Results from this study support that FA can provide useful, additional information besides visual evaluation alone on a reproducible manner. However, prospective studies are needed to optimize the best use of this technology for this indication and to determine standards for the interpretation of FA images and the potential subsequent need for second-look surgeries.