Role of imaging in the applicability of irreversible electroporation for the management of pancreatic adenocarcinoma

Luiz Tenório Siqueira de Brito Correspondence: Dr. Luiz Tenório Siqueira de Brito. Departamento de Radiologia - Hospital Vila Nova Star. Rua Doutor Alceu de Campos Rodrigues, 126, Vila Nova Conceição. São Paulo, SP, Brazil, 04544-000. Email: luiz.bsiqueira@oncologiador.com.br.

Hospital Vila Nova Star, Rede D’Or, São Paulo, SP, Brazil

http://orcid.org/0000-0002-9013-666X

Correspondence: Dr. Luiz Tenório Siqueira de Brito. Departamento de Radiologia - Hospital Vila Nova Star. Rua Doutor Alceu de Campos Rodrigues, 126, Vila Nova Conceição. São Paulo, SP, Brazil, 04544-000. Email: luiz.bsiqueira@oncologiador.com.br.

Figures (11)
Tables (3)

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Figure 1
Representation of the American Joint Committee on Cancer international system of classification of tumors(²2 Amin MB, Edge SB, Greene FL, et al., editors. AJCC cancer staging manual. 8th ed. Chicago, IL: American College of Surgeons; 2017.), based on imaging assessment of the tumor (T), lymph nodes (N), and metastases (M). (CA, celiac artery; SMA, superior mesenteric artery; CHA, common hepatic artery).

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Figure 2
Intraoperative IRE.

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Figure 3
Vascular anatomy relevant to pancreatic adenocarcinoma.

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Figure 4
Axial maximum intensity projection reconstruction of a contrast-enhanced CT scan of the abdomen, showing a pancreatic tumor in a 61-year-old man. There is contact (< 180°) between the tumor and the superior mesenteric artery (SMA), with amputation of the inferior pancreaticoduodenal artery (IPDA, first branch of the SMA). Borderline-resectable tumor. IRE was used as an adjuvant intraoperative technique.

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Figure 5
Axial contrast-enhanced CT scan of the abdomen, in the arterial phase, showing a tumor in the pancreatic body in a 78-year-old man. A comparison between the imaging aspects of the acquisition with a dual-energy protocol depicting the tumor in contact (> 180°) with the celiac artery and in marginal contact with the abdominal aorta. Unresectable tumor. The dual-energy technique increases the contrast between different tissues by processing a set of acquisitions at different voltages. Benefits over the conventional technique include better differentiation between the tumor and healthy pancreatic parenchyma, optimized vascular assessment, reduced tomographic beam attenuation artifacts caused by metallic materials (e.g., surgical clips and biliary stents), and improved image quality when the acquisition is suboptimal (e.g., reduced renal or cardiac function, which alter the circulation dynamics of iodinated contrast in the bloodstream). IRE was performed as a stand-alone procedure.

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Figure 6
Axial contrast-enhanced CT scan of the abdomen, in a maximum intensity projection, showing a tumor (T) in the pancreatic body in a 69-year-old woman, in contact (> 180°) with the celiac artery and the common hepatic artery. Unresectable tumor. Involvement of the splenic artery, with caliber reduction, and splenic vein thrombosis are also observed. IRE was used as a stand-alone procedure, in combination with chemoradiotherapy.

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Figure 7
Axial contrast-enhanced CT scan of the abdomen (A), in the portal phase, and axial magnetic resonance imaging scan of the abdomen (B), in 3D T1-weighted sequence, showing a tumor (T) in the head of the pancreas in contact (< 180°) with the spleno-mesenteric junction in a 67-year-old woman. Note the focal tapering and irregular contours of the tumor. Borderline-resectable tumor. IRE was performed intraoperatively as an adjuvant procedure.

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Figure 8
Unenhanced CT scan of the abdomen, showing an expansile tumor (T) in the tail of the pancreas, involving the splenic artery, as well as occluding the splenic vein and left renal vein, in an 89-year-old woman. Resectable tumor. The patient had an unfavorable performance status, with multiple comorbidities, and surgery was contraindicated due to high surgical risk. As a therapeutic alternative, CT-guided IRE was used as an exclusive procedure, in combination with chemotherapy.

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Figure 9
Axial contrast-enhanced CT scans of the abdomen, in the portal phase, showing a tumor, centered in the head and uncinate process of the pancreas, in a 69-year-old man. Note the extensive involvement of local anatomical structures, especially the gastric wall and the third portion of the duodenum. The tumor was also in contact (> 180°) with the superior mesenteric artery and the common hepatic artery. There were also liver metastases. Unresectable tumor. Involvement of hollow viscera walls represents a contraindication to IRE (risk of perforation). In this case, it was possible to perform CT-guided stand-alone IRE based on confirmation by endoscopic ultrasound that the wall infiltration was segmental, with integrity of some layers. Although duodenal or gastric involvement is not one of the criteria of the American Joint Committee on Cancer TNM system, evidence in the literature indicates that it is an isolated factor with an impact on disease survival(¹¹11 Dal Molin M, Blackford AL, Siddiqui A, et al. Duodenal involvement is an independent prognostic factor for patients with surgically resected pancreatic ductal adenocarcinoma. Ann Surg Oncol. 2017;24:2379-86.).

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Figure 10
Contrast-enhanced abdominal CT scans, in the axial plane, showing a tumor [T] in the head of the pancreas, in a 79-year-old man, with extensive local involvement, highlighting infiltration of the second portion of the duodenum, the common hepatic artery, and the proper hepatic artery. Endoscopic ultrasound could facilitate the evaluation of infiltration of the layers of the duodenal wall, which represents a contraindication to IRE. Note also the malignant obstruction of the bile ducts, a complication occasionally observed in PDAC and that requires treatment with a biliary stent before IRE can be performed, because of the risk that the edema generated by the procedure will worsen the obstruction.

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Figure 11
Flow chart of practices in PDAC, highlighting the role of IRE.

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Table 1
Staging of PDAC, based on the tumor-node-metastasis system outlined in the Cancer Staging Manual of the American Joint Committee on Cancer, 8th edition(²2 Amin MB, Edge SB, Greene FL, et al., editors. AJCC cancer staging manual. 8th ed. Chicago, IL: American College of Surgeons; 2017.).

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Table 2
Surgical classification and resectability criteria for pancreatic cancer(¹1 Kulkarni NM, Soloff EV, Tolat PP, et al. White paper on pancreatic ductal adenocarcinoma from society of abdominal radiology’s disease-focused panel for pancreatic ductal adenocarcinoma: Part I, AJCC staging system, NCCN guidelines, and borderline resectable disease. Abdom Radiol (NY). 2020;45:716-28.).

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Table 3
Proposal by Fromer et al.(⁹9 Fromer MW, Hawthorne J, Philips P, et al. An improved staging system for locally advanced pancreatic cancer: a critical need in the multidisciplinary era. Ann Surg Oncol. 2021;28:6201-10.) for the classification of locally advanced (stage III) PDAC, analyzed together with the application of IRE proposed in the present study for management of the disease.

Category	PDAC stage
Category	IA	IB	IIA	IIB	III	III	IV
T	T1	T2	T3	T1-T3	T4	T1-T4	T1-T4
N	N0	N0	N0	N1	N0-N2	N2	N0-N2
M	M0	M0	M0	M0	M0	M0	M1

	Vascular structures		Resectable	Borderline resectable	Unresectable
Vascular structures	Venous	Portal vein or superior mesenteric vein	No contact Contact < 180° without contour irregularities	Contact > 180° Contact < 180° with deformity/ thrombosis, not precluding resection or reconstruction Contact with the inferior vena cava	Involvement precluding resection or reconstruction Contact with proximal jejunal drainage branches
	Arterial	Common hepatic artery	No contact	Contact, without extension to the celiac artery or the hepatic bifurcation	Extension to the celiac artery/ hepatic bifurcation
		Celiac artery	No contact	No contact (head) Contact < 180° (body/tail)	Contact > 180°^f
		Superior mesenteric artery	No contact	Contact < 180°	Contact > 180° Contact with the first jejunal branch of the superior mesenteric artery
		Aorta	No contact	No contact	Any contact
		Anatomical variants^* * A tumor in contact with arterial anatomical variants may be considered borderline resectable depending on the experience of the surgeon(s).	None	Right accessory hepatic artery or artery of aberrant origin (variable degree of contact)^* * A tumor in contact with arterial anatomical variants may be considered borderline resectable depending on the experience of the surgeon(s).	-
Other structures		-	-	-	Metastasis (including distal lymph nodes)

Parameter	Classification system proposed by Fromer et al.(⁹9 Fromer MW, Hawthorne J, Philips P, et al. An improved staging system for locally advanced pancreatic cancer: a critical need in the multidisciplinary era. Ann Surg Oncol. 2021;28:6201-10.)				Proposed application of IRE
Parameter	> 180° arterial involvement	Subclassification	Resectability		Aplicability	Objective
With or without venous involvement (of the portal vein or superior mesenteric vein) that does not preclude reconstruction	Celiac artery or common hepatic artery	IIIa	Possible (modified Appleby procedure)^* * En bloc resection of the celiac artery with anastomosis between the common hepatic artery and the gastroduodenal artery, to maintain hepatic and gastroduodenal flow. Commonly, there is resection of the distal pancreas and spleen.	⇒	Intraoperative	Resection with tumor-free margins
	Superior mesenteric artery	IIIb1	Low^* * En bloc resection of the celiac artery with anastomosis between the common hepatic artery and the gastroduodenal artery, to maintain hepatic and gastroduodenal flow. Commonly, there is resection of the distal pancreas and spleen.	⇒	Intraoperative or stand-alone	Resection with tumor-free margins Local control; positive impact on morbidity and mortality
	Celiac artery + superior mesenteric artery	IIIb2	Very low (selected cases)^†	⇒	Intraoperative or stand-alone
With venous involvement (of the portal vein or superior mesenteric vein) that precludes reconstruction	No arterial involvement	IIIc1	Not viable^§ § The surgical complexity represented by involvement of multiple vessels makes resection unfeasible in these situations, except under circumstances of scientific/experimental investigation.	⇒	Stand-alone	Local control; positive impact on morbidity and mortality
	Celiac artery	IIIc2
	Superior mesenteric artery	IIIc3
	Celiac artery + superior mesenteric artery	IIIc4

[1] Correspondence: Dr. Luiz Tenório Siqueira de Brito. Departamento de Radiologia - Hospital Vila Nova Star. Rua Doutor Alceu de Campos Rodrigues, 126, Vila Nova Conceição. São Paulo, SP, Brazil, 04544-000. Email: luiz.bsiqueira@oncologiador.com.br.

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Role of imaging in the applicability of irreversible electroporation for the management of pancreatic adenocarcinoma

Abstract