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Role of indo-cyanine green (ICG) fluorescence in laparoscopic adrenalectomy: a retrospective review of 55 Cases
Eham Arora1 . Ajay Bhandarwar1 . Amol Wagh1 . Saurabh Gandhi1 . Chintan Patel1 . Shubham Gupta1 . Gagandeep Talwar1 . Jasmine Agarwal1 . Jai Rathore1 . Soumya Chatnalkar1
Received: 10 April 2018 / Accepted: 18 June 2018 @ Springer Science+Business Media, LLC, part of Springer Nature 2018
Abstract
Background Indo-Cyanine Green Fluorescence is an emerging technology with more frequent use in laparoscopic and robotic surgery. It relies on near-infrared (NIR) fluorescence to demonstrate tissue perfusion with demarcation of tissue planes and vascular pedicles. The aim of the study is to evaluate the role of this technology in laparoscopic adrenalectomy (LA). Methods 55 patients underwent laparoscopic adrenalectomy using NIR Fluorescence enabled laparoscope. All cases received a standard initial dose of 5-mg dye to aid tissue visualization. Surgery proceeded with “fluorescence mode” demonstrating real-time NIR images superimposed on standard white-light imaging. The timing, number of doses were dictated by the operating surgeon, which were recorded and correlated with intra-operative fluorescence visualization.
Results 54 patients underwent successful LA, with one conversion in a case of large pheochromocytoma due to difficult hemostasis. The lag between ICG administration and visualization of adrenal fluorescence varied between 30 and 75 s. The total duration of adrenal parenchymal fluorescence after a single dose did not exceed 15 min in our series. Average total administered dose was 14.4 mg. We suffered no mortality. There were no adverse effects due to the dye. 5 patients suffered Grade I complications, with one patient suffering Grade II and IV complication each, as per Clavien-Dindo Classifica- tion. Final histopathology demonstrated pheochromocytoma, adrenocortical adenoma, adrenocortical carcinoma, cushing’s adenoma, aldosteronoma, and myelolipoma.
Conclusion We describe our initial positive experience with ICG fluorescence in LA, with a detailed description of dye administration in our study. The technology offers real-time differentiation of tissues and identification of vascular structures, providing immediate guidance during surgery. Further evaluation of its role in adrenocortical malignancy is warranted. NIR fluorescence is a safe, useful addition in laparoscopic adrenalectomy which will undergo further refinement over time.
Keywords Laparoscopic adrenalectomy . Adrenalectomy · Indo-cyanine green . Fluorescence angiography · Near-infrared imaging
Transabdominal & retroperitoneal “open” adrenalectomy (OA) was the standard of care for adrenal lesions for most of the twentieth century. We witnessed a tectonic shift towards laparoscopic adrenalectomy (LA) after it was first described in 1992 [1]. It has remained the gold standard for benign adrenal lesions ever since. LA seemed an obvious improvement over conventional “open” technique with lower
morbidity, mortality, intra-operative blood loss, hospital stay, faster convalescence and improved cosmesis. Over the next two decades, multiple centers reaffirmed these benefits [2-6]. As adrenalectomies constituted a small fraction of a laparoscopic surgeon’s practice, it was suggested the proce- dure be performed at specialist centers by those proficient at advanced laparoscopy [7]. With growing experience, the procedure was also adapted to a single-port technique [8]. The next incremental improvement was the use of robotics with a further improvement in hospital stay, blood loss, and post-operative complications [9-11].
Indo-Cyanine Green (ICG) fluorescence technology has gradually crept into laparoscopy, offering real-time fluores- cence angiography and assessment of vascular status of both
☒ Eham Arora ehamarora@gmail.com
1 Department of General Surgery, Grant Government Medical College & Sir JJ Group of Hospitals, 6th floor, Hospital Building, Sir JJ Hospital Campus, Sir JJ Marg, Byculla, Mumbai 400008, India
hollow and solid organs [12]. Early in its deployment, the technology was found to be most useful in hepato-biliary surgery owing to its excretion via this organ system [13]. As with any new technology, researchers are discovering newer applications for it with a continual assessment of benefit gained.
The aim of this study is to evaluate the role of ICG fluo- rescence in laparoscopic adrenalectomy.
Materials and methods
Between December 2016 and January 2018, 55 consecutive patients underwent unilateral laparoscopic adrenalectomy using Pinpoint Endoscopic Fluorescence Imaging System (Novadaq, Mississauga, Ontario, Canada) at Sir JJ Hospi- tal, by the minimal access surgical unit consisting of three operating surgeons with individual experience with LA exceeding 20 cases. Selection criteria are stated in Table 1. Institutional ethics approval was obtained for the study and informed consent was obtained from each participating patient.
ICG administration
Every patient was given an intradermal test dose of 0.1 mg ICG on the ventral aspect of their right forearm a day prior to surgery, to rule out any allergic reactions. In patients with large tumors without anatomical distortion, dissec- tion progressed as per standard technique of LA. When tis- sue planes became indistinct, an intravenous dose of 5 mg ICG diluted in 10 cc distilled water was administered by
Table 1 Selection Criteria of patients for laparoscopic adrenalectomy using ICG fluorescence enabled laparoscope
Selection criteria of patients
Inclusion criteria
1 18 years of age or older
2. Consenting to be a part of the study
3. Secretory adrenal tumors of any size
4. Non-secretory adrenal tumors less than 10 cm in size
Exclusion criteria
1. Age less than 18 years
2. Not consenting to be a part of the procedure
3. Unfit for general anesthesia
4. Previous adrenal surgery
5. Suspicion of local invasion or vascular infiltration on imaging studies
6. Prior history of drug anaphylaxis
7. Allergic response to test dose of ICG given prior to surgery
8. Pregnancy
the anesthesiologist over 5 s. For smaller lesions or when tissue planes were vague, the initial dose were administered earlier during dissection. Subsequent doses were adminis- tered at the discretion of the operating surgeon. The ICG dose, number of doses and stage of surgery at which they were administered were noted.
Operative visualization
The camera mode was changed to “fluorescence” mode on administration of ICG. The Pinpoint system allows simul- taneous, real-time fluorescence imaging superimposed on standard white-light imaging (Fig. 1). This is achieved via rapid alternation between xenon white light and near-infra- red light by the system. The result is a vivid reproduction of the green fluorescence of ICG against a high-definition full color visualization of the operative field. The “Spy” mode offered by the system depicts the fluorescence of ICG within tissues as white against a dark gray background (Fig. 2). After specimen placement in retrieval bags in vivo, residual ICG fluorescence within it, if any, was noted along with the time since previous ICG dose prior to disconnection of vascular pedicles.
Operative technique
Standard 4-port transabdominal LA was performed in all cases with patients in lateral or semi-lateral position. Har- monic shears and bipolar vessel sealing devices were used with standard laparoscopic instrumentation for dissection.
Results
Patient demography
A total 55 patients underwent unilateral LA at our center over 2 years. The group consisted of 35 (63.7%) men and 20 (36.3%) women. Their average age was 38.2 years with an average BMI of 26.5 kg/sq m. 31 patients (56.4%) suf- fered from right adrenal lesions and 24 (43.6%) possessed left adrenal pathologies. Clinically, the group comprised 17 cases of pheochromocytomas, 5 cases of aldosteronomas, 4 cases of Cushing’s syndrome, and 29 “indeterminate” non-functioning adrenal masses. Final histopathological analysis of these masses revealed 1 pheochromocytoma, 23 adrenocortical adenomas, 3 adrenocortical carcinomas, and 2 myelolipomas.
Surgical outcome
A single conversion (1.8%) occurred in a case with a 6.5- cm left adrenal pheochromocytoma due to difficulty in
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hemostasis. The mean operative time of the remaining 54 patients was 129.8 min. Average operating time was 123 min for right-sided lesions and 139 min for left-sided lesions. Average intra-operative blood loss was 82 ml (range 50 to 680 ml).
ICG dosing
The average total ICG dose administered per case was 14.4 mg (range 7.5 to 22.5 mg). A standard 5 mg initial dose was administered to all patients. In 21 (38.2%) cases,
this first dose was administered after reflection of bowel, but prior to commencement of adrenal dissection. The average gland size in this group was 3.2 cm. In the remain- ing 32 (61.8%) patients, the first dose was administered after adrenal dissection was already underway. The lag between ICG administration and visualization of adrenal
fluorescence varied between 30 and 75 s. The bright angio- graphic “inflow” visualization of pedicles lasted less than 30 s (Figs. 3, 4) with a more gradual venous outflow visu- alization up to 90 s after ICG administration (Fig. 5). The total duration of adrenal parenchymal fluorescence did not exceed 15 min in our series.
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Complications
We suffered no mortality in our series. No patient exhib- ited any allergic reaction to ICG pre- or post-operatively. Complications were graded as per Clavien-Dindo classifi- cation (Table 2) [14]. Five (9.1%) patients suffered grade I complications of post-operative ileus, urinary retention or stitch abscess. A single patient (1.8%) suffered a grade II complication in the form of intra-operative blood loss need- ing a blood transfusion. One case (1.8%) suffering from a
pheochromocytoma had a turbulent intra-operative course necessitating extended post-operative stay in an intensive care unit (Grade IV complication).
Discussion
Over the past two decades, researchers have noted a substan- tial increase in annual rate of adrenalectomies. Moreover, a larger fraction of those with doubtful diagnosis of adrenal
| Grade | Definition |
|---|---|
| Grade I | Any deviation from the normal post-operative course without the need for pharmacological treat- ment or surgical, endoscopic, and radiological interventions |
| Grade II | Requiring pharmacological treatment with drugs other than such allowed for grade I complications |
| Grade III | Requiring surgical, endoscopic or radiological intervention |
| Grade IIIa | Intervention not under general anesthesia |
| Grade IIIb | Intervention under general anesthesia |
| Grade IV | Life-threatening complication (including CNS complications)ª requiring IC/ICU management |
| Grade IVa | Single organ dysfunction (including dialysis) |
| Grade IVb | Multiorgan dysfunction |
| Grade V | Death of a patient |
| Suffix "d" | If the patient suffers from a complication at the time of discharge, the suffix "d" (for "disability") is added to the respective grade of complication. This label indicates the need for a follow-up to fully evaluate the complication |
CNS central nervous system, IC intermediate care, ICU intensive care unit
aBrain hemorrhage, ischemic stroke, subarachnoid bleeding, but excluding transient ischemic attacks
lesions have undergone surgery. This trend has largely been attributed to improvements in radio-imaging aiding diagno- sis, with a widespread adoption of LA by laparoscopic sur- geons [15-17]. While LA has been applied to early malig- nant adrenal lesions with some success, it is usually termed a “gold standard” for “benign” lesions [5, 6]. Most stud- ies evaluating the efficacy of LA have excluded cases with suspicion of adrenal malignancy on radio-imaging. Lesions larger than 6 cm, or those with metastatic deposits elsewhere were generally not offered LA. Even so, in most series, final histopathology often revealed an unsuspected adrenocortical malignancy [4, 7, 18, 19].
An increase in non-functioning adrenal lesion size is associated with progressively higher risk of malignancy. However, a cut-off of 6 cm size for LA, as advised by most researchers [20-22], will still be met by an occasional inva- sive malignancy. It is therefore essential to follow oncologic surgical principles in every LA. Indeed, researchers have achieved some success in LA for suspected adrenocortical malignancies in the absence of local invasion or vascular infiltration [23]. Machado et al. have found no significant dif- ferences in outcome between OA and LA across all stages of adrenocortical malignancy [24]. Notably, they state “A poor outcome is likely to result from inadequate surgery, irrespec- tive of whether the approach is open or laparoscopic.”
Indo-Cyanine Green is a sterile, anionic, water-soluble dye which was developed by Kodak Laboratories in 1955. When injected intravenously, it remains largely confined to the vascular compartment due to its binding to plasma proteins. It is eliminated by rapid hepatic uptake and bil- iary excretion in unchanged form. ICG was approved by the FDA for medical use in 1959, and first found application in ophthalmology for retinal angiography, where has remained a mainstay for decades. ICG demonstrates blood vessels in deeper tissue planes than those visually apparent, as it oper- ates in the near-infrared (NIR) spectrum in which tissues are more translucent [13]. Tissues are illuminated with light possessing a wavelength of 750-800 nm, corresponding to the excitation wavelength of the dye [25]. A camera with the required filters can display the NIR fluorescence of dye within tissues. This is performed in real-time, allowing the fluorescence data to be super-imposed over standard visual image. As techniques and technology improved, ICG was cleared by the FDA for cerebral and coronary angiography in 2003 and 2005 respectively [26, 27]. The technology has been applied to enhance anatomical visualization in surgery, determine hepatic reserve in cirrhosis prior to resection, and cardiac output monitoring [13, 28-30].
ICG’s foray into laparoscopy found early application in cholecystectomy owing to its clearance in bile [31]. It allows focused visualization of the biliary tree, to potentially reduce the risk of common bile duct injury [32, 33]. NIR fluores- cence has moved out of its niche and become a mainstream
technology with advancements in minimal access surgery. It serves as a valuable tool in a specialty where the surgeon is limited in his/her direct contact with tissues, helping make intra-operative assessments and aiding decision-making. Owing to its pharmacokinetics, the specifics of intra-oper- ative ICG administration change with the organ system. Delineation of tissue planes, correct identification, and sub- sequent division of vascular pedicles (Figs. 6, 7), ensuring a complete resection without residual tumor, are essential components of any LA. These steps of the procedure have the potential to be aided by ICG Fluorescence technology. Dip et al. first demonstrated the feasibility of adrenal visu- alization at laparoscopy using ICG in a large animal model [34]. Manny et al. tested this hypothesis in humans in three consecutive patients with solitary adrenal lesions [35]. They successfully performed robotic trans-peritoneal partial adre- nalectomy with negative margins with 5 mg of intravenous ICG aiding identification of gland. DeLong et al. found vivid enhancement of adrenal vessels with clear demarcation of adrenal gland and adjacent tissues in their series of four laparoscopic adrenalectomies using NIR Fluorescence [36]. Further evaluation of technology in robotic adrenalectomy by Colvin et al. found that ICG fluorescence imaging was superior or equivalent to standard laparoscopic visualization in 72.1% of their cases [37]. Importantly, they determined that ICG imaging was particularly superior for adrenocorti- cal tumors. While Sound et al. have described the manner of ICG administration in robotic adrenalectomy, with rec- ommendations for its dose and timing, no such description exists in a larger series of laparoscopic adrenalectomies.
Within our series of 55 cases, all three operating surgeons unanimously agreed that ICG fluorescence routinely helped improve the course of surgery. In patients with smaller glands, ICG helps differentiate between the adrenal gland and surrounding retro-peritoneal fat. The former has a vivid uptake of the dye. This initial demarcation of site and extent of gland helps commence dissection. The adrenal gland has multiple vascular pedicles, and their accurate identification is central to ensuring hemostasis. This is particularly true of large, vascular adrenal tumors. In such cases, differen- tiating the gland from surrounding adipose tissue is simple task. The first dose of ICG in such cases was given either when tissue planes became indistinct or when vascular chan- nels needed identification. In large lesions where anatomi- cal distortion has occurred, and there exists an uncertainty regarding division of all vascular pedicles, the lack of fluo- rescence within the gland after ICG administration provides an indirect confirmation of the same. The only caveat to this method is allowing residual fluorescence from previous dose to subside, which occurs within 15 min. The short duration of fluorescence within the gland means a single dose of ICG cannot provide fluorescence for the entirety of the opera- tion, no matter how skilful or speedy the surgeon may be.
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The average number of doses received over the course of LA was 3.2 (range 2 to 6), with an average dose of 14.4 mg (range 7.5-22.5 mg). This is well below the level of 5 mg/ kg dose deemed safe [13, 38]. ICG has been documented to cause anaphylaxis, bronchospasm and skin eruptions, but the incidence is extremely low [39, 40]. We did not witness any such adverse effects in our series.
The presence of the liver above the right adrenal gland poses a challenge due to strong hepatic fluorescence in the operative field, which can mask adrenal enhancement. We have employed generous hepatic retraction with instruments during use of “fluorescence” mode, along with zooming in on the adrenal gland to reduce the fraction of liver visualized in the NIR image. In patients suffering from adrenocortical
carcinoma and myelolipoma, the afflicted part of the gland exhibits hypofluorescence when compared to the rest. It was this property that enabled Manny et al. to perform par- tial adrenalectomies after distinguishing between normal and pathological portions of the gland. However, it is our interpretation that NIR fluorescence may not greatly benefit patients with adrenocortical malignancy. This is based on our observation of hypofluorescence within the gland in the three cases operated, which was also noted by Sound et al. in their short series of robotic adrenalectomies [41]. Although we achieved a negative margin in our series, there is scope for incomplete resection when relying on information from fluorescence. This is due to a contrasting dye uptake between malignant and benign lesions within the adrenal gland. A larger series of malignancies subjected to ICG fluorescence may held shed further light on this contentious issue.
In tumors creeping onto the renal hilum, the angiographic phase of ICG fluorescence helps identify a clear plane of dissection between the structures. This was particularly help- ful in one patient whose right renal vessels were flanked by pheochromocytoma above and a paraganglioma below. The lack of NIR fluorescence in loose areolar tissue between enhancing glands and vessels contributes to the surgeon’s confidence while dissecting, helping reduce operative times.
NIR fluorescence is finding its way into more operating rooms, before clinicians have had an opportunity to fully comprehend its application. This is apparent by the num- ber of publications, like this one, which acknowledge its suitability to a procedure, but cannot quantify the benefits gained. This would be best served by a randomized control trial comparing laparoscopic adrenalectomies performed with and without NIR fluorescence, but the paucity of cases is a strong limitation.
Conclusion
We report our experience with NIR Fluorescence using ICG in 55 cases of laparoscopic adrenalectomy. The surgi- cal team acknowledges the utility of the technology in real- time differentiation of tissues and identification of vascular structures, providing immediate guidance during surgery. NIR Fluorescence is a dynamic tool, the effects of which are improved with timely dye administration. This timing is largely reliant on the organ being operated and the astute- ness of the operating team. The technology is not without its shortcomings-its role in right adrenalectomy is blunted due to hepatic fluorescence, and its suitability to adrenocortical carcinomas due to hypofluorescence of the lesion cannot be commented upon in a small series. NIR fluorescence is a safe, useful addition in laparoscopic adrenalectomy which will undergo further refinement over time.
Compliance with ethical standards
Disclosures The authors would like to state that this manuscript is being submitted as an accompaniment to podium presentation at SAGES 2018, held at Seattle, USA titled “Use of IndoCyanine Green (ICG) Fluorescence in Laparoscopic Adrenalectomy.” Program num- ber: S135 (Solid Organ Session). Eham Arora, Ajay Bhandarwar, Amol Wagh, Saurabh Gandhi, Chintan Patel, Shubham Gupta, Gagandeep Talwar, Jasmine Agarwal, Jai Rathore, Soumya Chatnalkar have no conflict of interest or financial ties to disclose.
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