Label-Free Enhancement of Adrenal Gland Visualization Using Near-Infrared Autofluorescence for Surgical Guidance.


Journal

World journal of surgery
ISSN: 1432-2323
Titre abrégé: World J Surg
Pays: United States
ID NLM: 7704052

Informations de publication

Date de publication:
02 2023
Historique:
accepted: 03 09 2022
pubmed: 3 10 2022
medline: 4 1 2023
entrez: 2 10 2022
Statut: ppublish

Résumé

During adrenalectomy, surgeons have traditionally relied on their subjective visual skills to distinguish adrenal glands (AGs) from retroperitoneal fat and surrounding structures, while ultrasound and exogenous contrast agents have been employed for intraoperative AG visualization, all of which have their limitations. We present a novel label-free approach that uses near-infrared autofluorescence (NIRAF) detection, which demonstrates potential for enhanced intraoperative AG visualization and efficient tumor resection during adrenalectomies. Patients undergoing adrenalectomy or nephrectomy were enrolled for this feasibility study. NIRAF emitted beyond 800 nm was detected in vivo from AGs and surrounding tissues during open adrenalectomies or nephrectomies. NIRAF was also measured ex vivo in excised AGs following robotic adrenalectomies. NIRAF images of tissues were captured using near-infrared (NIR) camera systems, whereas NIRAF intensities were recorded concurrently using fiber-optic probe-based NIR devices. Normalized NIRAF intensities (expressed as mean ± standard error) were analyzed and compared. Among the 55 enrolled patients, NIRAF intensity was elevated significantly for AGs versus retroperitoneal fat and other structures. NIR images of AGs also revealed a distinct demarcation of NIRAF between adrenal cortex and other periadrenal structures. NIRAF intensity in AGs was decreased markedly in malignant adrenal tumors, while benign adrenal cortical tumors and healthy adrenal cortex exhibited the strongest NIRAF levels. Our preliminary findings indicate that NIRAF detection could be a promising label-free technology to enhance intraoperative AG visualization and holds immense potential for effective tumor demarcation during cortical-sparing adrenalectomies or adrenal-conserving surgeries.

Sections du résumé

BACKGROUND
During adrenalectomy, surgeons have traditionally relied on their subjective visual skills to distinguish adrenal glands (AGs) from retroperitoneal fat and surrounding structures, while ultrasound and exogenous contrast agents have been employed for intraoperative AG visualization, all of which have their limitations. We present a novel label-free approach that uses near-infrared autofluorescence (NIRAF) detection, which demonstrates potential for enhanced intraoperative AG visualization and efficient tumor resection during adrenalectomies.
METHODS
Patients undergoing adrenalectomy or nephrectomy were enrolled for this feasibility study. NIRAF emitted beyond 800 nm was detected in vivo from AGs and surrounding tissues during open adrenalectomies or nephrectomies. NIRAF was also measured ex vivo in excised AGs following robotic adrenalectomies. NIRAF images of tissues were captured using near-infrared (NIR) camera systems, whereas NIRAF intensities were recorded concurrently using fiber-optic probe-based NIR devices. Normalized NIRAF intensities (expressed as mean ± standard error) were analyzed and compared.
RESULTS
Among the 55 enrolled patients, NIRAF intensity was elevated significantly for AGs versus retroperitoneal fat and other structures. NIR images of AGs also revealed a distinct demarcation of NIRAF between adrenal cortex and other periadrenal structures. NIRAF intensity in AGs was decreased markedly in malignant adrenal tumors, while benign adrenal cortical tumors and healthy adrenal cortex exhibited the strongest NIRAF levels.
CONCLUSIONS
Our preliminary findings indicate that NIRAF detection could be a promising label-free technology to enhance intraoperative AG visualization and holds immense potential for effective tumor demarcation during cortical-sparing adrenalectomies or adrenal-conserving surgeries.

Identifiants

pubmed: 36184672
doi: 10.1007/s00268-022-06755-y
pii: 10.1007/s00268-022-06755-y
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

350-360

Subventions

Organisme : NCI NIH HHS
ID : R01 CA212147
Pays : United States

Informations de copyright

© 2022. The Author(s) under exclusive licence to Société Internationale de Chirurgie.

Références

Boland GWL, Blake MA, Hahn PF et al (2008) Incidental adrenal lesions: principles, techniques, and algorithms for imaging characterization. Radiology 249:756–775
doi: 10.1148/radiol.2493070976
Low G, Dhliwayo H, Lomas DJ (2012) Adrenal neoplasms. Clin Radiol 67:988–1000
doi: 10.1016/j.crad.2012.02.005
Mansmann G, Lau J, Balk E et al (2004) The clinically inapparent adrenal mass: update in diagnosis and management. Endocr Rev 25:309–340
doi: 10.1210/er.2002-0031
Young WF (2007) The incidentally discovered adrenal mass. N Engl J Med 356:601–610
doi: 10.1056/NEJMcp065470
Mazzaglia PJ, Varghese J, Habra MA (2020) Evaluation and management of adrenal neoplasms: endocrinologist and endocrine surgeon perspectives. Abdominal Radiology 45:1001–1010
doi: 10.1007/s00261-020-02464-z
Hergus S, Lynn J (1993) Surgical anatomy and surgery of the adrenal gland. Surg Endocrinol 1:458–467
Prager G, Heinz-Peer G, Passler C et al (2002) Surgical strategy in adrenal masses. Eur J Radiol 41:70–77
doi: 10.1016/S0720-048X(01)00441-7
Uludağ M, Aygün N, İşgör A (2020) Surgical Indications and Techniques for Adrenalectomy. Sisli Etfal Hastan Tip Bul 54:8–22
Agrusa A, Romano G, Navarra G et al (2017) Innovation in endocrine surgery: robotic versus laparoscopic adrenalectomy. Meta-analysis and systematic literature review. Oncotarget 8:102392–102400
doi: 10.18632/oncotarget.22059
Sound S, Okoh AK, Bucak E et al (2016) Intraoperative tumor localization and tissue distinction during robotic adrenalectomy using indocyanine green fluorescence imaging: a feasibility study. Surg Endosc 30:657–662
doi: 10.1007/s00464-015-4256-0
Ikeda Y, Takami H, Niimi M et al (2001) Laparoscopic partial or cortical-sparing adrenalectomy by dividing the adrenal central vein. Surg Endosc 15:747–750
doi: 10.1007/s004640080112
Brunt LM, Bennett HF, Teefey SA et al (1999) Laparoscopic ultrasound imaging of adrenal tumors during laparoscopic adrenalectomy. Am J Surg 178:490–494
doi: 10.1016/S0002-9610(99)00220-2
Siperstein AE, Berber E, Engle KL et al (2000) Laparoscopic posterior adrenalectomy: technical considerations. Arch Surg 135:967–971
doi: 10.1001/archsurg.135.8.967
Lucas SW, Spitz JD, Arregui ME (1999) The use of intraoperative ultrasound in laparoscopic adrenal surgery. Surg Endosc 13:1093–1098
doi: 10.1007/s004649901180
Ashitate Y, Levitz A, Park MH et al (2016) Endocrine-specific NIR fluorophores for adrenal gland targeting. Chem Commun 52:10305–10308
doi: 10.1039/C6CC03845J
Obermeyer RJ, Knauer EM, Millie MP et al (2003) Intravenous methylene blue as an aid to intraoperative localization and removal of the adrenal glands during laparoscopic adrenalectomy. Am J Surg 186:531–534
doi: 10.1016/j.amjsurg.2003.07.011
Amin Nasr A, Fatani J, Kashkari I et al (2009) Use of methylene blue in pheochromocytoma resection: case report. Paediatr Anaesth 19:396–401
doi: 10.1111/j.1460-9592.2009.02956.x
Manny TB, Pompeo AS, Hemal AK (2013) Robotic partial adrenalectomy using indocyanine green dye with near-infrared imaging: the initial clinical experience. Urology 82:738–742
doi: 10.1016/j.urology.2013.03.074
DeLong JC, Chakedis JM, Hosseini A et al (2015) Indocyanine green (ICG) fluorescence-guided laparoscopic adrenalectomy. J Surg Oncol 112:650–653
doi: 10.1002/jso.24057
Colvin J, Zaidi N, Berber E (2016) The utility of indocyanine green fluorescence imaging during robotic adrenalectomy. J Surg Oncol 114:153–156
doi: 10.1002/jso.24296
Rossi L, Fregoli L, De Palma A et al (2021) Retroperitoneoscopic cortical sparing adrenalectomy with indocyanine green fluorescence. Videoscopy 31:1
doi: 10.1089/vor.2021.0023
Gasparella P, Singer G, Arneitz C et al (2021) Indocyanine green-guided adrenal sparing laparoscopic resection of a recurrent pheochromocytoma with a concurrent ganglioneuroma (composite Pheochromocytoma–Ganglioneuroma) in a Girl with von Hippel-Lindau Disease. Videoscopy 31:1
doi: 10.1089/vor.2020.0712
Hope-Ross M, Yannuzzi LA, Gragoudas ES et al (1994) Adverse Reactions due to Indocyanine Green. Ophthalmology 101:529–533
doi: 10.1016/S0161-6420(94)31303-0
McWade MA (2016) Development of an intraoperative tool to detect parathyroid gland autofluorescence. Vanderbilt University
Paras C, Keller M, Mahadevan-Jansen A et al (2011) Near-infrared autofluorescence for the detection of parathyroid glands. J Biomed Opt 16:067012
doi: 10.1117/1.3583571
Thomas G, McWade MA, Sanders ME, et al (2016) Identifying the novel endogenous near-infrared fluorophore within parathyroid and other endocrine tissues. Biomedical Optics Conference, Fort Lauderdale, Florida, Optica Publishing Group, PTu3A.5
Scoville S, Miller BS, Dedhia PH et al (2021) Near-infrared autofluorescence of adrenal glands. J Am Coll Surg 233:S67
doi: 10.1016/j.jamcollsurg.2021.07.119
Thomas G, McWade MA, Nguyen JQ et al (2019) Innovative surgical guidance for label-free real-time parathyroid identification. Surgery 165:114–123
doi: 10.1016/j.surg.2018.04.079
Thomas G, Squires MH, Metcalf T et al (2019) Imaging or fiber probe-based approach? assessing different methods to detect near infrared autofluorescence for intraoperative parathyroid identification. J Am Coll Surg 229:596-608.e593
doi: 10.1016/j.jamcollsurg.2019.09.003
Squires MH, Jarvis R, Shirley LA et al (2019) Intraoperative parathyroid autofluorescence detection in patients with primary hyperparathyroidism. Ann Surg Oncol 26:1142–1148
doi: 10.1245/s10434-019-07161-w
Thomas G, McWade MA, Paras C et al (2018) Developing a clinical prototype to guide surgeons for intraoperative label-free identification of parathyroid glands in real time. Thyroid 28:1517–1531
doi: 10.1089/thy.2017.0716
Lupo J, Kemp J, Paquette I et al (2008) Trends in adrenal surgery and adrenal cancer incidence and survival in the era of laparoscopic surgery. J Am Coll Surg 207:S79
doi: 10.1016/j.jamcollsurg.2008.06.197
Kaye DR, Storey BB, Pacak K et al (2010) Partial adrenalectomy: underused first line therapy for small adrenal tumors. J Urol 184:18–25
doi: 10.1016/j.juro.2010.03.052
Noureldine SI, Nazli Avci S, Isiktas G, et al (2022) Detection of near‐infrared autofluorescence from adrenal neoplasms: An initial experience. J Surg Oncol (e-pub):1–6
Moore EC, Rudin A, Alameh A et al (2019) Near-infrared imaging in re-operative parathyroid surgery: first description of autofluorescence from cryopreserved parathyroid glands. Gland Surg 8:283–286
doi: 10.21037/gs.2018.12.05
Angelousi A, Szarek E, Shram V et al (2017) Lipofuscin Accumulation in Cortisol-Producing Adenomas With and Without PRKACA Mutations. Horm Metab Res 49:786–792
doi: 10.1055/s-0043-116385
Cheng B, Tserng KY, Kowal J et al (1996) Characterization and identification of an adrenal age-related nonpolar fluorescent substance. Endocrinology 137:2447–2456
doi: 10.1210/endo.137.6.8641198
Mochizuki Y, Park MK, Mori T et al (1995) The Difference in Autofluorescence Features of Lipofuscin between Brain and Adrenal. Zoolog Sci 12(283–288):286
Kovacs K, Horvath E, Feldman PS (1976) Pigmented adenoma of adrenal cortex associated with Cushing’s syndrome: light and electron microscopic study. Urology 7:641–645
doi: 10.1016/0090-4295(76)90094-7
Taubitz T, Fang Y, Biesemeier A et al (2019) Age, lipofuscin and melanin oxidation affect fundus near-infrared autofluorescence. EBioMedicine 48:592–604
doi: 10.1016/j.ebiom.2019.09.048
Kahramangil B, Kose E, Berber E (2018) Characterization of fluorescence patterns exhibited by different adrenal tumors: Determining the indications for indocyanine green use in adrenalectomy. Surgery 164:972–977
doi: 10.1016/j.surg.2018.06.012

Auteurs

Giju Thomas (G)

Vanderbilt Biophotonics Center, Vanderbilt University, Nashville, TN, 37235, USA.
Department of Biomedical Engineering, Vanderbilt University, Nashville, TN, 37235, USA.

Colleen M Kiernan (CM)

Division of Surgical Oncology and Endocrine Surgery, Department of Surgery, Vanderbilt University Medical Center, 1211 Medical Center Drive, Nashville, TN, 37232, USA.

Parker A Willmon (PA)

Vanderbilt Biophotonics Center, Vanderbilt University, Nashville, TN, 37235, USA.
Department of Biomedical Engineering, Vanderbilt University, Nashville, TN, 37235, USA.

Ezekiel Haugen (E)

Vanderbilt Biophotonics Center, Vanderbilt University, Nashville, TN, 37235, USA.
Department of Biomedical Engineering, Vanderbilt University, Nashville, TN, 37235, USA.

Amy N Luckenbaugh (AN)

Division of Urologic Oncology, Department of Urology, Vanderbilt University Medical Center, Nashville, TN, 37232, USA.

Daniel A Barocas (DA)

Division of Urologic Oncology, Department of Urology, Vanderbilt University Medical Center, Nashville, TN, 37232, USA.

Naira Baregamian (N)

Division of Surgical Oncology and Endocrine Surgery, Department of Surgery, Vanderbilt University Medical Center, 1211 Medical Center Drive, Nashville, TN, 37232, USA.

Anita Mahadevan-Jansen (A)

Vanderbilt Biophotonics Center, Vanderbilt University, Nashville, TN, 37235, USA.
Department of Biomedical Engineering, Vanderbilt University, Nashville, TN, 37235, USA.

Carmen C Solόrzano (CC)

Division of Surgical Oncology and Endocrine Surgery, Department of Surgery, Vanderbilt University Medical Center, 1211 Medical Center Drive, Nashville, TN, 37232, USA. carmen.solorzano@vumc.org.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH