Circulatory Engagement of Abdominal Inconstant Preexisting Arterial Collaterals, as Revealed by MSCT Angiography, Indicates Unresectability of Pancreatic Cancer

Objective. To assess the prognostic value of the collateral flow through abdominal inconstant arterial collateral pathways of persistent primary origin, as defined with MSCT angiography (MSCTA), in terms of its providing one of the criteria for resectability of pancreas cancer. Material and methods. Both retrospective and prospective analyses of the diagnostic and treatment outcomes data from 837 patients who had presented to Vishnevsky Surgery Institute between 2008 and 2013 were conducted with evaluation of diagnostic accuracy of MSCT. 627 (74.9%) out of them made up the screening group (controls), the group of operated subjects comprised 85 (10.2%) patients who had undergone different types of radical pancreatic surgery with resection of the great arteries. A group of 98 (11.7%) patients had pancreatic tumors deemed unresectable by MSCT. There were also 27 (3.2%) cases of nontumor-related celiac artery stenosis. Intravenous boluscontrast-enhanced MSCT with post-processing of MSCTA data was performed on a Brilliance 64-Slice CT scanner or a Brilliance iCT 256-Slice CT system (Phillips, Cleveland, OH, USA) using a bolus-tracking technique: 2D multiplanar and 3D MSCTA reconstructions were generated with the Brilliance Workspace Portal (Philips Medical Systems), ARIS MultiVox version 5 (the Medical Computer Systems Laboratory at the Lomonosov Moscow State University’s Skobeltsyn Institute of Nuclear Physics). Results. In our unresectable pancreatic cancer patients 1. aberrant arterial anatomy was 2-2.5 times more commonly found and 2. follow-up MSCT showed the pattern of the celiac-mesenteric arterial vasculature to be changed by the presence of pancreatic tumor in such a way where the variant artery acted as a collateral. Not a single collateral artery was encountered in 20.4% of our cases of non-resectable pancreatic cancer. In most of the unresectable pancreatic cancer patients, no fewer than 2-3 collateral channels were seen. The occurrence of the left type collateral arcades was demonstrated to be 60.2% in the group of unresectable tumors. The MSCT achieved an accuracy of 100% in correctly identifying the celiac-mesenteric arterial vasculature type. There were no discrepancies between the imaging and intraoperative findings. Conclusions. In the setting of tumor involvement of the celiac-mesenteric territories’ major arteries, the accessoryhepatic arteries serve as collaterals routes. Functional inconstant preexisting abdominal arterial collaterals as depicted by MSCTA are a sign of invasion of the wall of a great vessel, evidence of their recruitment is highly indicative of pancreatic cancer unresectability. Altered Michels’ type of the celiac-mesenteric arterial architecture in non-resectable pancreas cancer suggests that the type of the celiac-mesenteric arterial anatomy cannot be presumed consistent at all times. Its estimation only holds true at the time of scanning. Detection of the left type collateral arcades significantly reduces the chance of pancreatic tumor resection.

резектабельность опухолей поджелудочной железы, артерии поджелудочной железы, артериальные коллатерали брюшной полости, типы строения артерий целиако-мезентериального бассейна по Michels, pancreatic cancer resectability, arteries of the pancreas, abdominal arterial collaterals, Michels’ types of the celiac-mesenteric arterial anatomy

1. Simard E.P., Ward E.M., Siegel R., Jemal A. Cancers with increasing incidence trends in the United States: 1999 through 2008. Cancer J. Clin.. 2012; 62 (2): 118-128.

2. Siegel R., Naishadham D., Jemal A. Cancer statistics, 2013. Cancer J. Clin. 2013; 63 (1): 11-30.

3. Каприн А.Д., Старинский В.В., Петрова Г.В. Состояние онкологической помощи населению России в 2014 году. М.: ФГБУ “МНИОИ им. П.А. Герцена” Минздравa России. 2014. http://www.oncology.ru/service/statistics/

4. Hirota M., Shimada S., Yamamoto K. et al. Pancreatectomy using the no-touch isolation technique followed by extensive intraoperative peritoneal lavage to prevent cancer cell dissemination: a pilot study. JOP. 2005; 6 (2): 143-151.

5. Esposito I., Kleeff J., Bergmann F. et al. Most pancreatic cancer resections are R1 resections. Ann. Surg. Oncol. 2008; 15 (6): 1651-1660.

6. Захарова О.П. Компьютерно-томографические признаки резектабельности рака поджелудочной железы: Автореф. дис …. канд. мед. наук. М., 2012. 25 с.

7. Walker T.G. Mesenteric vasculature and collateral pathways. Seminars in interventional radiology. Thieme Medical Publishers. 2009; 26 (3): 167.

8. Hardman R.L., Lopera J.E.., Cardan R.A. et al. Common and Rare Collateral Pathways in Aortoiliac Occlusive Disease: A Pictorial Essay. Am. J. Roentgenol. 2011; 197: W519-W524.

9. Kosaka M., Horiuchi K., Nishida K. et al. Hepatopancreatic arterial ring: bilateral symmetric typology in human celiaco-mesenteric arterial system. Acta Med. Okayama. 2012; 56 (5): 245-254.

10. Song S.-Y., Chung J.W., Yin Y.H. et al. Celiac Axis and Common Hepatic Artery Variations in 5002 Patients: Systematic Analysis with Spiral CT and DSA1. Radiology. 2010; 255 (1): 278-288.

11. Horton K.M., Fishman E.K. Volume-rendered 3D CT of the Mesenteric Vasculature: Normal Anatomy, Anatomic Variants, and Pathologic Conditions. Radiographics. 2002; 22 (1): 161-172.

12. Michels N.A. Newer anatomy of the liver and its variant blood supply and collateral circulation. Am. J. Surg. 1966; 112 (3): 337-347.

13. Benoit G., Bensadoun H., Moukarzel M. et al. Anatomical basis of whole pancreas transplantation. Surg. Radiol. Anat. 1989; 11 (3): 181-185.

14. Michels N.A. Blood supply and anatomy of the upper abdominal organs with a descriptive atlas. Philadelphia (Pa). USA: Lippincott, 1955. 581 p.

15. Kimura W. Surgical anatomy of the pancreas for limited resection. J. Hepatobiliary Pancreat. Surg. 2000; 7: 473-479.

16. Копчак В.М., Усенко А.Ю., Копчак К.В., Зелинский А.И. Хирургическая анатомия поджелудочной железы. Киев: Аскания, 2011: 23-43.

17. Prager R.J., Akin J.R., Akin G.C., Binder R.J. Winslow's pathway: a rare collateral channel in infrarenal aortic occlusion. Am. J. Roentgenol. 1977; 128 (3): 485-487.

18. Sebastià C., Quiroga S., Boyé R. et al. Aortic Stenosis: Spectrum of Diseases Depicted at Multisection CT. Radiographics. 2003; 23 (Suppl. 1): S79-S91.

19. Kim J., Won J.Y., Park S.I., Lee D.Y. Internal thoracic artery collateral to the external iliac artery in chronic aortoiliac occlusive disease. Korean J. Radiol. 2003 jul-sept; 4 (3): 179-183.

20. Sakorafas G.H., Sarr M.G., Peros G. Celiac artery stenosis: an underappreciated and unpleasant surprise in patients undergoing pancreaticoduodenectomy. J. Am. Coll. Surg. 2008; 206 (2): 349-356.

21. Yi S.Q., Li J., Terayama H. et al. A rare case of inferior mesenteric artery arising from the superior mesenteric artery, with a review of the review of the literature. Surg. Radiol. Anat. 2008; 30 (2): 159-165.

22. Hardman R.L., Lopera J.E., Cardan R.A. et al. Common and rare collateral pathways in aortoiliac occlusive disease: a pictorial essay. Am. J. Roentgenol. 2011; 197 (3): W519-W524.

23. Мирошников Б.И., Горбунов Г.Н., Иванов А.П. Пластика пищевода. СПб.: ЭЛБИ-СПб, 2012: 69-81.

24. Долго-Сабуров Б.А. Анастомозы и пути окольного кровообращения у человека. 3-е изд., перераб. и доп. Л.: Медгиз, 1956. 142 с.

25. Jiji P.J., D’Costa S., Nayak S.R. et al. An anamolous digestive arterial anastomosis connecting foregut, midgut and hind gut. Trakya Univ. Tip. Fak. Dergesi. 2008; 25 (3): 241-244.

26. Сосудистая хирургия по Хаймовичу. В 2-х томах. Под ред. Э.М. Ашера. М.: БИНОМ. Лаборатория знаний, 2010; Т. 1: 122-137.

27. Фениш Х. Карманный атлас анатомии человека на основе Международной номенклатуры; Пер. под ред. С.Д. Денисова. Минск: Высшая школа, 1997. 464 с.

28. Niculescu M.C., Niculescu V., Ciobanu I.C. et al. Correlations between the colic branches of the mesenteric arteries and the vascular territories of the colon Romanian. J. Morphol. Embryol. 2005; 46 (3): 193-197.

29. Адамская Н.А., Цыганков В.Н., Косова И.А. КТ-ангиография в планировании лоскутов передней брюшной стенки. Пластическая хирургия и косметология. 2010; 4: 571-575.

30. Kalva S.P., Athanasoulis C.A., Greenfield A.J. et al. Inferior pancreaticoduodenal artery aneurysms in association with celiac axis stenosis or occlusion. Eur. J. Vasc. Endovasc. Surg. 2007; 33 (6): 670-675.

31. Michels N.A. Collateral arterial pathways to the liver after ligation of the hepatic artery and removal of the celiac axis. Cancer. 1953; 6: 708-724.

32. Plengvanit U., Chearanai O., Sindhvananda K. et al. Collateral arterial blood supply of the liver after hepatic artery ligation, angiographic study of twenty patients. Ann. Surg. 1972; 175 (1): 105-110.

33. Koehler R.E., Korobkin M., Lewis F. Arteriographic demonstration of collateral arterial supply to the liver after hepatic artery ligation. Radiology. 1975; 117 (10): 49-54.

34. Charnsangavej C. et al. Angiographic classification of hepatic arterial collaterals. Radiology. 1982; 144 (3): 485-494.

35. Tohma T., Cho A., Okazumi S. et al. Communicating Arcade between the Right and Left Hepatic Arteries: Evaluation with CT and Angiography during Temporary Balloon Occlusion of the Right or Left Hepatic Artery 1. Radiology. 2005; 237 (1): 361-365.

36. Kim H.C., Chung J.W., Lee W. et al. Recognizing Extrahepatic Collateral Vessels That Supply Hepatocellular Carcinoma to Avoid Complications of Transcatheter Arterial Chemoembolization 1. Radiographics. 2005; 25 (suppl. 1): S25-S39.

37. Gunji H., Cho A., Tohma T. et al. The blood supply of the hilar bile duct and its relationship to the communicating arcade located between the right and left hepatic arteries. Am. J. Surg. 2006; 192 (3): 276-280.

38. Cho A., Gunji H., Koike N. et al. Intersegmental arterial communication between the medial and left lateral segments of the liver. Dig. Surg. 2007; 24: 328-330.

39. Hirano S., Kondo S., Tanaka E. et al. Safety of combined resection of the middle hepatic artery in right hemihepatectomy for hilar biliary malignancy. J. Hepatobiliary Pancreat. Surg. 2009; 16 (6): 796-801.

40. Arias F.J., Martín M.B., Pinheiro da Silva N. et al. Extrahepatic vessels depending on the hepatic artery. Identification and management. Radiología (Eng. Ed.). 2011; 53 (1): 18-26.

41. Балахнин П.В. Значение вариантов артериальной анатомии печени для выполнения интервенционно-радиологических вмешательств: Автореф. дис. ... канд. мед. наук. Санкт-Петербург, 2012. 21 с.

42. Gwon D.I., Ko G.Y., Yoon H.K. et al. Inferior Phrenic Artery: Anatomy, Variations, Pathologic Conditions, and Interventional Management1. Radiographics. 2007; 27 (3): 687-705.

43. Tanaka R., Ibukuro K., Akita K. The left inferior phrenic artery arising from left hepatic artery or left gastric artery: radiological and anatomical correlation in clinical cases and cadaver dissection. Abdom. Imaging. 2008; 33 (3): 328-333.

44. Topaz O. Origin of a common trunk for the inferior phrenic arteries from the right renal artery: a new anatomic vascular variant with clinical implications. Cardiovasc. Rev. Med. 2010; 11 (1): 57-62.

45. Khamanarong K., Woraputtaporn W., Amarttayakong P. et al. The right ovarian artery arising from the right inferior phrenic artery: a case report. J. Med. Assoc. Thai. 2012; 95 (5): 743-745.

46. Wirtanen G.W., Kaude J.V. Inferior phrenic artery collateralization in hepatic artery occlusion. Radiology. 1973; 117 (3): 615-619.

47. Wilcox P., Baile E.M., Hards J. et al. Phrenic nerve function and its relationship to atelectasis after coronary artery bypass surgery. Chest. J. 1988; 93 (4): 693-698.

48. Jung J.W., Hwang S., Namgoong J.M. et al. Incidence and management of postoperative abdominal bleeding after liver transplantation. Transplant. Proc. 2012; 44 (3): 765-768.

49. Cohen A.M., Higgins J., Waltman A.C. et al. Effect of ligation of variant hepatic arterial structures on the completeness of regional chemotherapy infusion. Am. J. Surg. 1987; 153 (4): 378-380.

50. Burke D., Earlam S., Fordi C., Allen-Mersh T.G. Effect of aberrant hepatic arterial anatomy on tumor response to hepatic artery infusion of floxuridine for colorectal liver metastases. Br. J. Surg. 1995; 82 (8): 1098-1100.

51. Lee D. H., Hwang J.C., Lim S.M. et al. Pleural and pulmonary staining at inferior phrenic arteriography mimicking a tumor staining of hepatocellular carcinoma. Cardiovasc. Intervent. Radiol. 2000; 23 (2): 109-113.

52. Miyayama S., Matsui O., Taki K. et al. Transcatheter arterial chemoembolization for hepatocellular carcinoma fed by the reconstructed inferior phrenic artery: anatomical and technical analysis. J. Vasc. Intervent. Radiol. 2004; 15 (8): 815-823.

53. Прокоп М., Галански М. Спиральная и многослойная компьютерная томография. В 2-х томах. М.: МЕДпресс-информ, 2011; Т. 2: 307-323.

54. Miyayama S., Yamashiro M., Yoshie Y. et al. Inferior phrenic arteries: angiographic anatomy, variations, and catheterization techniques for transcatheter arterial chemoembolization. Jap. J. Radiology. 2010; 28 (7): 502-511.

55. Song S.Y., Chung J.W., Kwon J.W. et al. Collateral pathways in patients with celiac axis stenosis: angiographic-spiral CT correlation. Radiographics. 2002; 22 (4): 881-893.

56. Douard R., Chevallier J.M., Delmas V. et al. Clinical interest of digestive arterial trunk anastomoses. Surg. Radiol. Anat. 2006; 28 (3): 219-227.

57. Song S.Y., Chung J.W., Yin Y.H. et al. Celiac Axis and Common Hepatic Artery Variations in 5002 Patients: Systematic Analysis with Spiral CT and DSA1. Radiology. 2010; 255 (1): 278-288.

58. Балахнин П.В., Таразов П.Г. Классификация вариантов артериального кровоснабжения печени для рентгенэндоваскулярных вмешательств: анализ результатов 3756 ангиографий. Анналы хирургической гепатологии. 2014; 19 (2): 24-42.

59. El-Ghazaly Harb S.T., O'Sullivan A.W., Marangoni G. et al. Managing Arterial Collaterals Due to Coeliac Axis Stenosis During Pancreaticoduodenectomy. J. Pancreas (Online). 2009; 10 (5): 547-549.

60. Вольф К.Ю. Лучевая диагностика. Артерии и вены. М.: МЕДпресс-информ, 2011: 239-242.

61. Shukla P.J., Barreto S.G., Kulkarni A. et al. Vascular anomalies encountered during pancreatoduodenectomy: do they influence outcomes? Ann. Surg. Oncol. 2010; 17 (1): 186-190.

62. Lai E. Vascular resection and reconstruction at pancreatico-duodenectomy: technical issues. Hepatobiliary & Pancreatic Dis. Int. 2012; 11 (3): 234-242.

63. Boggi U., Del Chiaro M., Croce C. et al. Vascular complications of pancreatectomy. J. Pancreas (Online). 2007; 8 (1): 102-113.

64. Allendorf J.D., Bellemare S. Reconstruction of the replaced right hepatic artery at the time of pancreaticoduodenectomy. J. Gastrointest. Surg. 2009; 13: 555-557.

65. Seelig M. H., Belyaev O., Uhl W. Reconstruction of the common hepatic artery at the time of total pancreatectomy using a splenohepatic bypass. J. Gastrointest. Surg. 2010; 14 (5): 913-915.