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CLINICAL ANATOMY. Revista Română de Anatomie funcţională şi clinică, macro- şi microscopică şi de Antropologie. Vol. XIV Nr.

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Vol. XIV – Nr. 3 – 2015 CLINICAL ANATOMY

PreservATION Of AN ACCessOrY LefT HePATIC

ArTerY DurINg rADICAL gAsTreCTOMY fOr CANCer –

Is IT ONCOLOgICALY sAfe?

Al. Martiniuc1, v. Herlea2, Mirela Boros3, M. Ionescu1, T. Dumitrascu1 1. Center of General Surgery and Liver Transplant

2. Department of Pathology 3. Fundeni Clinical Institute, Bucharest

Department of Radiology

PReSeRvaTIon oF an aCCeSSoRy LeFT HePaTIC aRTeRy DuRInG RaDICaL GaS-TReCTomy FoR CanCeR – IS IT onCoLoGICaLy SaFe? (abstract): Background/ aim: an accessory left hepatic artery (aLHa) is sometimes observed during surgery for gastric cancer. However, the clinical significance of the preservation/ division of an aLHa during radical gas-trectomies is poorly investigated. The aim of the present study is to assess the incidence and oncological safety of the preservation of an aLHa during D2 gastrectomy for gastric cancer, in a single surgical team experience. Patients and methods: The study cohort included 159 patients with D2 gastrectomies (2004 – 2015). Results: a D2 total gastrectomy was performed in 132 patients (83%). Splenectomy was associated in 55 patients (35%) while a distal pancreatectomy was performed in 9 patients (5.6%). The 90-day mortality rate was 5%. a postoperative pancre-atic fistula was the most frequently encountered complication – 17 patients (10.6%). Preservation of an aLHa was considered in only 3 patients (1.8%). The number of the harvested lymph nodes in the group of patients with aLHa preservation was 20, 68 and 71, respectively. Conclusion: Preservation of an aLHa during D2 gastrectomy is rarely necessary because its division is almost never followed by clinically significant consequences. However, whenever preservation of an aHLa is considered, this procedure is technically feasible, without jeopardizing the oncological safety of a radical gastrectomy for cancer. Key words: aCCeSSoRy LeFT HePaTIC aRTeRy, D2 GaSTReCTomy, GaSTRIC CanCeR

INTrODuCTION

a D2 gastrectomy is considered nowadays the standard curative-intent surgery for advanced gastric cancers (i.e., tumors beyond the mus-cularis propria or with loco-regional lymph nodes metastases, but without distant metasta-ses), particularly in east asian countries(1).

In Western surgical centers, the benefit of a D2 over a D1gastrectomy is still controversial. Thus, the initial results of the Dutch rand-omized trial did not show any survival benefit but increased morbidity and mortality rates for the D2 gastrectomies in gastric cancer(2). Sim-ilar results were also shown in the uK rand-omized trial(3). However, the long-term results of the Dutch trial have shown that a D2 gas-trectomy is associated with significantly

de-creased loco-regional recurrence and gastric-cancer-related death rates, compared with the D1 gastrectomies(4). Furthermore, a recent Italian randomized study has shown that a D2 gastrec-tomy might potentially have a benefit in patients with advanced gastric cancer and lymph nodes metastases, without increased morbidity and mortality rates, compared with the D1 gastrec-tomies(5). These data recommend the use of a D2 gastrectomy in resectable gastric cancer if performed in high-volume centers(4). never-theless, it is worth to mention that the Italian study did not show any 5-year overall survival benefit for the D2 gastrectomies, compared with the D1 resections(5).

In our surgical center, based on the experience learned from the Japanese surgical teams(6),

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we have started to use the D2 gastrectomies for resectable gastric cancer, with significantly im-proved survivals rates, compared with the D1 resections (median survival time 78 vs. 28 months), without increased morbidity or mor-tality rates(7). The feasibility of a minimally-invasive approach for these patients was also demonstrated in our center(8;9).

an accessory left hepatic artery (aLHa) with origin from the left gastric artery is some-times observed during surgery for gastric can-cer. a radical gastrectomy formally implies the division of the left gastric artery at its origin. However, the clinical significance of the pres-ervation/ division of an aLHa during radical gastrectomies is poorly investigated.

The aim of the present study is to assess the incidence and oncological safety of the preser-vation of an aLHa during D2 gastrectomy for gastric cancer, in a single surgical team experi-ence.

PATIeNTs AND MeTHODs

The study cohort included 159 D2 gastrec-tomies for gastric cancer performed in the Center of General Surgery and Liver Transplant, Fundeni Clinical Institute, Bucharest, Romania by a sin-gle surgical team, which included, alternative-ly, two first operative surgeons (mI and TD). on notice, the cohort included the learning curve for D2 gastrectomy for one of the first operative surgeons (TD).

a D2 gastrectomy was considered according to the Japanese Gastric Cancer association definitions (1). Thus, a D2 gastrectomy in-cluded a total/ distal resection of the stomach, omentectomy, bursectomy, and removal of the following lymph nodes groups(1):

• 1-7, 8a, 9, 10, 11p, 11d and 12a (for total gastrectomies)

• 1-7, 8a, 9, 11p and 12a (for distal gastrec -tomies).

Spleen and/or distal pancreas removal was considered only in patients with an intraopera-tive suspected tumor invasion of these organs. Furthermore, splenectomy was also performed for tumors located in the upper part of the stomach, even in the absence of tumor invasion.

Preservation of an aLHa was considered only in cases with a large diameter for aLHa and small-caliber for the left hepatic artery, thus, suggesting that an aLHa is potentially the main arterial source for the left liver.

Reconstruction after resection was made

us-ing a Roux-en-y esophago/ gastrojejunostomy. all the operations were performed by an open approach (xifo-umbilical midline incision).

an oncologically safe D2 gastrectomy was considered whenever the yield lymph nodes by the pathologist (vH) was at least 15, according to the widely accepted standards(10).

The postoperative mortality was defined as deaths occurring during the first 90 days after surgery. The postoperative pancreatic fistulae were considered according to the International Study Group for Pancreatic Surgery definition (11).

Statistical analysis

The data are presented as number (percent-ages). Comparisons between the groups were made using the Fisher’s test, two-tailed. P-values less than 0.05 were considered statisti-cally significant.

resuLTs

Operative data and postoperative outcomes a D2 total gastrectomy was performed in 132 patients (83%). Splenectomy was associ-ated in 55 patients (35%) while a distal pan-createctomy was performed in 9 patients (5.6%). all the operative specimens yield at least 15 lymph nodes, according to the pathology reports.

a postoperative pancreatic fistula was the most frequently encountered complication – 17 patients (10.6%). an esophagojejunostomy leakage was observed in 8 patients (5%). a re-laparotomy for complication was necessary for 12 patients (7.5%).

The 90-day mortality rate for the whole co-hort was 5%. a decreased mortality rate was observed during the period 2009 – 2015, com-pared with 2004 – 2008 (2% vs. 9%, p = 0.067).

Preservation of an ALHA during D2 gas-trectomy

Preservation of an aLHa was considered in only 3 patients (1.8%) (fig. 1 and 2). one patient (0.6%) presented associated replaced right hepatic artery with origin from the supe-rior mesenteric artery. The number of the har-vested lymph nodes in the group of patients with aLHa preservation was 20, 68 and 71, respectively.

DIsCussION

The early postoperative outcomes in the pre-sent series are similar to those reported in oth-ers recent series from Western high-volume

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centers for D2 gastrectomies(5;12). The rela-tively high mortality rate in the first period of the study (9%) might be explained by the fact that this period included the learning curve for D2 gastrectomy of one of the first operative surgeons. Lee and co-workers have demonstrat-ed that the learning curve for a qualifidemonstrat-ed sur-gery implies at least 23 D2 gastrectomies to be performed(13). In the present cohort of pa-tients, after the learning curve was reached for both first operative surgeons the mortality rate decreased to 2%. nevertheless, a mortality rate of 10% was previously reported for a D2 gas-trectomy(2;3).

The presence of an aLHa with origin from the left gastric artery in an adult is not uncom-mon, and it is due to the persistence of one of the two embryonic hepatic arteries(14). During the embryonic development, the left gastric artery divides into a transverse branch (i.e., gastric body artery) and an ascending branch (for the left liver)(15). Commonly, this ascend-ing branch became obliterated in adulthood; if not, it generates an aLHa(15).

Several studies have shown that an acces-sory or replaced left hepatic artery with origin from the left gastric artery is encountered in 6.6 – 34% of the cases(14;16-18). association of an aLHa with origin from the left gastric artery with a replaced right hepatic artery with origin from the superior mesenteric artery was reported in 0.4% of the cases(18). an excep-tional anatomical variant (0.16%) is a common hepatic artery with the origin from the left gastric artery(19). a preoperative computer

tomography angiography is a useful tool for the detection of an aLHa prior to gastrectomy for cancer(20).

an aLHa was considered in the past a limitation to perform a safe radical gastrectomy for cancer because its severance may lead to left liver necrosis requiring left hemi-hepatec-tomy, liver abscesses, cholangitis or acute liver failure(21-23). The presence of an aLHa might potentially increase the difficulty of other pro-cedures such as antireflux surgery(24).

It is the merit of Weimann and co-workers to demonstrate for the first time the feasibility and oncological safety of the aLHa preserva-tion during radical gastrectomy for cancer(25). Furthermore, other studies have shown similar results(17;26-30).

In current practice, an aLHa is usually divided during a D2 gastrectomy for cancer (17;28;31), as it was the case in the present study. Division of the aLHa has no clinically significant consequences except for temporar-ily elevated liver enzymes(17;24;28;30;31), a situation that might have a negative impact particularly in patients with a chronic liver disease(17). Thus, preservation of an aLHa should be considered only whenever the diam-eter of the vessel is larger than 2 mm and the left hepatic artery has a reduced caliber(15), with a special attention in patients with a chron-ic liver disease(17).

Shinohara and co-workers have shown that although the total number of harvested lymph nodes was significantly higher in patients with radical gastrectomies and a divided aLHa, fig. 1. Contrast-enhanced computed tomography showing an accessory left hepatic artery with origin

from the left gastric artery (a) frontal plane, (b) transverse plane (aLHa – accessory left hepatic artery; LGa – left gastric artery; CHa – common hepatic artery).

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compared with the patients with preserved aLHa, however no significant differences were observed between the groups for the number of harvested lymph nodes around the left gastric artery(30). Furthermore, no differences in the 5-year overall survival rates were observed be-tween the patients with and without aLHa preservation(30). In the present series, a sta-tistical comparison between the group of pa-tients with and without aLHa preservation was not possible due to the small number of patients with a preserved aLHa. However, in this latter group, in all the patients at least 20 lymph nodes were harvested by the pathologist and, thus the oncological safety was achieved, ac-cording to the widely accepted standards(10).

CONCLusION

Preservation of an aLHa during D2 gas-trectomy is rarely necessary because its divi-sion is almost never followed by clinically significant consequences. However, whenever preservation of an aHLa is considered, this procedure is technically feasible, without jeop-ardizing the oncological safety of a radical gas-trectomy for cancer.

ACKNOWLeDgeMeNTs

The data of the present paper were pre-sented at the 16th national Congress of the Romanian Society of anatomy (may 8, 2015, Bucharest, Romania).

fig. 2. a preserved accessory left hepatic artery with origin from the left gastric artery after a D2 total gastrectomy – intraoperative aspects (aLHa – accessory left hepatic artery; LGa – left gastric artery; CHa – common hepatic artery; LHa – left hepatic artery; GDa – gastroduodenal artery; Sa –

splen-ic artery; CT – celiac trunk).

refereNCes

1. Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer 2011 Jun;14(2):113-23. 2. Bonenkamp JJ, Hermans J, Sasako m, van de velde CJ, Welvaart K, Songun I, et al. extended

lymph-node dissection for gastric cancer. N Engl J Med 1999 mar 25;340(12):908-14.

3. Cuschieri a, Weeden S, Fielding J, Bancewicz J, Craven J, Joypaul v, et al. Patient survival after D1 and D2 resections for gastric cancer: long-term results of the mRC randomized surgical trial. Surgical Co-operative Group. Br J Cancer 1999 mar;79(9-10):1522-30.

4. Songun I, Putter H, Kranenbarg em, Sasako m, van de velde CJ. Surgical treatment of gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol 2010 may;11(5):439-49.

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5. Degiuli m, Sasako m, Ponti a, vendrame a, Tomatis m, mazza C, et al. Randomized clinical trial comparing survival after D1 or D2 gastrectomy for gastric cancer. Br J Surg 2014 Jan;101(2):23-31. 6. vasilescu C, Trandafir B. [Current problems in surgical oncology 2. a lesson from Japan. D2

lym-phadenectomy in gastric cancer]. Chirurgia (Bucur) 2011 mar;106(2):163-70.

7. vasilescu C, Herlea v, Tidor S, Ivanov B, Stanciulea o, manuc m, et al. [D2 lymph node dissection in gastric cancer surgery: long term results--analysis of an experience with 227 patients]. Chirurgia (Bucur) 2006 Jul;101(4):375-84.

8. vasilescu C, Procopiuc L. Robotic surgery of locally advanced gastric cancer: a single-surgeon expe-rience of 41 cases. Chirurgia (Bucur ) 2012 Jul;107(4):510-7.

9. vasilescu C, Popa m, Tudor S, manuc m, Diculescu m. Robotic surgery of locally advanced gastric cancer -- an initial experience. Acta Chir Belg 2012 may;112(3):209-12.

10. Schwarz Re. Current status of management of malignant disease: current management of gastric can-cer. J Gastrointest Surg 2015 apr;19(4):782-8.

11. Bassi C, Dervenis C, Butturini G, Fingerhut a, yeo C, Izbicki J, et al. Postoperative pancreatic fis-tula: an international study group (ISGPF) definition. Surgery 2005 Jul;138(1):8-13.

12. Kung CH, Lindblad m, nilsson m, Rouvelas I, Kumagai K, Lundell L, et al. Postoperative pancreatic fistula formation according to ISGPF criteria after D2 gastrectomy in Western patients. Gastric Cancer 2014;17(3):571-7.

13. Lee JH, Ryu KW, Lee JH, Park SR, Kim CG, Kook mC, et al. Learning curve for total gastrectomy with D2 lymph node dissection: cumulative sum analysis for qualified surgery. Ann Surg Oncol 2006 Sep;13(9):1175-81.

14. abid B, Douard R, Chevallier Jm, Delmas v. [Left hepatic artery: anatomical variations and clinical implications]. Morphologie 2008 Dec;92(299):154-61.

15. Guadagni S, maruyama K, Sano T, Kinoshita T, marsili L, valenti m, et al. Pre-operative angiography in gastric cancer surgery with extended lymphadenectomy. Hepatogastroenterology 1999 Jul;46(28): 2701-9.

16. Hiatt JR, Gabbay J, Busuttil RW. Surgical anatomy of the hepatic arteries in 1000 cases. Ann Surg 1994 Jul;220(1):50-2.

17. Huang Cm, Chen Qy, Lin JX, Zheng CH, Li P, Xie JW, et al. Short-term clinical implications of the accessory left hepatic artery in patients undergoing radical gastrectomy for gastric cancer. PLoS One 2013;8(5):e64300.

18. Kobayashi S, otsubo T, Koizumi S, ariizumi S, Katagiri S, Watanabe T, et al. anatomic variations of hepatic artery and new clinical classification based on abdominal angiographic images of 1200 cases. Hepatogastroenterology 2014 nov;61(136):2345-8.

19. Song Sy, Chung JW, yin yH, Jae HJ, Kim HC, Jeon uB, et al. Celiac axis and common hepatic artery variations in 5002 patients: systematic analysis with spiral CT and DSa. Radiology 2010 apr;255(1):278-88.

20. matsuki m, Kani H, Tatsugami F, yoshikawa S, narabayashi I, Lee SW, et al. Preoperative assessment of vascular anatomy around the stomach by 3D imaging using mDCT before laparoscopy-assisted gastrectomy. AJR Am J Roentgenol 2004 Jul;183(1):145-51.

21. Friesen SR. The significance of the anomalous origin of the left hepatic artery from the left gastric artery in operations upon the stomach and esophagus. Am Surg 1957 Dec;23(12):1103-8.

22. Hemming aW, Finley RJ, evans KG, nelems B, Fradet G. esophagogastrectomy and the variant left hepatic artery. Ann Thorac Surg 1992 Jul;54(1):166-8.

23. Lurie aS. The significance of the variant left accessory hepatic artery in surgery for proximal gastric cancer. Arch Surg 1987 Jun;122(6):725-8.

24. Klingler PJ, Seelig mH, Floch nR, Branton Sa, Freund mC, Katada n, et al. aberrant left hepatic artery in laparoscopic antireflux procedures. Surg Endosc 2004 may;18(5):807-11.

25. Weimann a, meyer HJ, mauz S, Ringe B, Jahne J, Pichlmayr R. [anatomic variations in the course of the left hepatic artery. a problem for systematic lymphadenectomy in gastrectomy or proximal stomach resection before stomach tube formation]. Chirurg 1991 Jul;62(7):552-6.

26. Celik a, Celik aS, altinli e, Beykal o, Caglayan K, Koksal n. Left gastric and right hepatic artery anomalies in a patient with gastric cancer: images for surgeons. Am J Surg 2011 aug;202(2):e13-e16. 27. Hagiwara a, Imanishi T, Sakakura C, otsuji e, Kitamura K, Itoi H, et al. Subtotal gastrectomy for

cancer located in the greater curvature of the middle stomach with prevention of the left gastric artery. Am J Surg 2002 Jun;183(6):692-6.

28. okano S, Sawai K, Taniguchi H, Takahashi T. aberrant left hepatic artery arising from the left gastric artery and liver function after radical gastrectomy for gastric cancer. World J Surg 1993 Jan;17(1):70-3.

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29. oki e, Sakaguchi y, Hiroshige S, Kusumoto T, Kakeji y, maehara y. Preservation of an aberrant hepatic artery arising from the left gastric artery during laparoscopic gastrectomy for gastric cancer. J Am Coll Surg 2011 may;212(5):e25-e27.

30. Shinohara T, ohyama S, muto T, yanaga K, yamaguchi T. The significance of the aberrant left he-patic artery arising from the left gastric artery at curative gastrectomy for gastric cancer. Eur J Surg Oncol 2007 oct;33(8):967-71.

31. Jeong Ga, Cho GS, Shin eJ, Lee mS, Kim HC, Song oP. Liver function alterations after laparosco-py-assisted gastrectomy for gastric cancer and its clinical significance. World J Gastroenterol 2011 Jan 21;17(3):372-8.

Corresponding author Traian Dumitrascu

Figure

fig. 2. a preserved accessory left hepatic artery with origin from the left gastric artery after a D2 total  gastrectomy – intraoperative aspects (aLHa – accessory left hepatic artery; LGa – left gastric artery;

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