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Year : 2018  |  Volume : 14  |  Issue : 12  |  Page : 1019-1023

Appleby operation for carcinoma of the body and tail of the pancreas

Department of Hepatobiliary Pancreatic Surgery, Henan Provincial People's Hospital, Zhengzhou 450003, China

Date of Web Publication11-Dec-2018

Correspondence Address:
Huan-Zhou Xue
Department of Hepatobiliary Pancreatic Surgery, Henan Provincial People's Hospital, Zhengzhou 450003
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0973-1482.199383

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 > Abstract 

Aims: The aim of this study is to evaluate the therapeutic efficacy of Appleby operation for carcinoma of the body and tail of pancreas.
Materials and Methods: From March 2010 to February 2015, Appleby operation was performed in 17 patients with carcinoma of the body and tail of pancreas. The values of fasting plasma blood, body weight (BW), visual analog pain intensity scale (VAS score), and the quality of life indices were evaluated before and 1 day, 1, 2, 6 weeks after surgery. Survival time, tumor recurrence time, hospitalization time, and treatment-related complications were analyzed.
Results: There was no hospital mortality. Pancreatic fistula and diarrhea were major and most frequent. The rate of morbidity in general was 47.1%. After operation, all of the patients were completely pain-free. The VAS score decreased more after surgery comparing with before (83.2 ± 8.5 vs. 1.9 ± 3.6, P < 0.05). After operation, patients gained more than their preoperative BW with a mean increment of (4.1 ± 1.3 kg) (68.1 ± 4.3 vs. 64.0 ± 6.7, P < 0.05). A significant rise of the overall quality of life index was observed after surgery (93.8 ± 9.7 vs. 68.6 ± 6.7, P < 0.05). The 1-, 2-, 3-, and 5-year recurrence rates were 22.9%, 58.9%, 72.6%, and 72.6%, respectively. The 1-, 2-, 3-, and 5-year survival rates after operation were 80.4%, 54.2%, 32.5%, and 16.3%, respectively.
Conclusions: Appleby operation is both safe and effective with regard to pain relief and improvement of overall quality of life. Appleby operation can also achieve a high survival rate and a long overall survival time.

Keywords: Body and tail of pancreas, carcinoma, pain, surgery

How to cite this article:
Shen Q, Jiang QF, Tian YW, Yu M, Jia JK, Xue HZ. Appleby operation for carcinoma of the body and tail of the pancreas. J Can Res Ther 2018;14, Suppl S5:1019-23

How to cite this URL:
Shen Q, Jiang QF, Tian YW, Yu M, Jia JK, Xue HZ. Appleby operation for carcinoma of the body and tail of the pancreas. J Can Res Ther [serial online] 2018 [cited 2020 Feb 26];14:1019-23. Available from: http://www.cancerjournal.net/text.asp?2018/14/12/1019/199383

 > Introduction Top

Since 1976,[1] Appleby's surgery was adopted for advanced pancreatic carcinoma of the body and tail by Nimura for the first time. From that time, the clinical study of modified Appleby in the treatment of pancreatic body and tail carcinoma has been gradually carried out all over the world.[2],[3],[4] Improved Appleby operation can significantly improve the R0 resection rate and effectively relieve the clinical symptoms of patients.[5],[6],[7] We performed a modified Appleby procedure for 17 patients with pancreatic body tail tumor, achieved good therapeutic effect, and reported as follows.

 > Materials and Methods Top


From March 2010 to February 2015, modified Appleby surgery was adopted in 17 cases of randomly selected patients with tumor of pancreatic body and tail. Among them, 10 cases were male and the other 7 were female. The age ranged from 46 to 69 years, with an average of 58 ± 8 years. Most of the patients were accompanied with an evident abdominal pain and back discomfort, ranging from 2 weeks to 3 months at night particularly. Eleven cases of patients had a history of taking analgesic drugs. All the enrolled cases were diagnosed with colored Doppler ultrasound and enhanced computed tomography (CT). Ultrasound showed a low echo mass in the tail of the pancreas body, with an unclear boundary and a uniform internal echo. Thin-section CT scans demonstrated a low attenuation with irregular-shaped (11 cases) and round and lobular (6 cases) mass. The maximum mean diameter was 5.4 ± 1 cm (95% confidence interval [CI]: 3.6–7.2 cm) [Figure 1]. Eight cases were diagnosed with a tumor invasion of hepatic artery combined with splenic artery, and five cases were celiac trunk and splenic artery invaded. The other four were diagnosed with splenic artery and left gastric artery. Laboratory examination revealed blood routine, liver and kidney function, and blood and urine amylase, clotting routine was in the range of reference values. Preoperative quality of life assessment and weight and pain visual analog scale (VAS) score are shown in [Table 1].
Figure 1: Recurrence and metastasis rate after operation

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Table 1: Changes of baseline data before and after surgery

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Surgical procedure

Cut the gastrocolic omentum and explore the tumor infiltrating. A whitish solid tumor taking up the whole of the pancreatic body and growing into the celiac axis (CA) trifurcation and common hepatic artery (CHA) with adherence to the left 180° of the uninvolved gastroduodenal artery was discovered. On duplex ultrasound with a clamp across the CHA, there was a sufficient arterial blood flow in the liver and the hepatic arterial pulsation was present as before. The lesion was judged resectable. A corpocaudal pancreatectomy with resection of the CA and its branches was completed. Moreover, then, stomach and spleen ligament was cutoff and the spleen was separated to the truncus coeliacus. Finally, we cut off celiac trunk and removed the tumor. Resection range: The body and tail of the pancreas, spleen, hepatic artery, left gastric artery, splenic artery, celiac trunk, retroperitoneal fascia tissue (including the celiac plexus, lymph nodes, etc.).


The indicators were liver function, fasting blood glucose, body weight, pain score, quality of life assessment, etc. Pain levels were evaluated by VAS.[8] No pain was given 0 point, mild pain was given <30 points, moderate pain was given 31–69 points, and severe pain was given more than 70 points. GIQLI was used to evaluate the quality of life;[9] it includes subjective symptoms, emotional, psychological, and physiological functions, social activities, and so on. A total of 36 survey projects were included and 0–4 points were recorded according to the actual. The maximum score on this test is 144, and higher than 125.8 points was recognized as normal. Two weeks and 6 weeks after surgery, the above indicators were evaluated and they were recommended to review regularly in the hospital once in a single year and once every 2 months in the 2nd year and one every 3 months in the 3rd year postoperatively, including liver function, blood and urine amylase, and tumor marker including carcinoembryonic antigen and CA199. Imaging examination such as abdominal colored Doppler ultrasound, chest X-ray, and upper abdominal enhancement CT was performed to understand whether the tumor had local recurrence or distant metastasis and to analyze the survival rate, etc.

Statistical analysis

Chi-square test and t-test were used for count data and measurement data, respectively. Kaplan–Meier analysis was used to analyze the survival rate. Log-rank test was used to evaluate the difference between groups. Taking α = 0.05 as benchmark.

 > Results Top

Pathological diagnosis was confirmed to be adenocarcinoma. Margin-positive (R1) was found in 2 cases of patients after sampling in multiple sites, including incisal margins of pancreas, celiac trunk, hepatic artery, and left gastric artery. Complete resection (R0) of the cancer was performed in the remaining 15 patients without residual tumor alone the incisal edge. The results of pathological examination: Highly, moderately, and poorly differentiated adenocarcinoma were found in 3, 8, and 4 cases, respectively. Moreover, one case was found of mucinous carcinoma and a single case of cystadenocarcinoma. Three cases of lymph node metastasis were found in the celiac trunk and hepatic artery. Lymph node metastasis in splenic artery and vein was found in three cases.


The patients in this group were operated successfully, and no death occurred during the perioperative period. The average time of stay in hospital was 11.9 + 3.4 days (7 days ~ 19 days, median length of stay in hospital 12 days). No liver abscess, liver function failure, ischemic stomach disease, peptic ulcer, upper gastrointestinal bleeding, and other potential postoperative complications were found during the perioperative period. One day after surgery, alanine transaminase (ALT), aspartate transaminase (AST), total bilirubin, and other indicators of liver function were significantly higher than the preoperative (P < 0.05) while the ALB was significantly lower (P < 0.05); one week after the operation, they were returned to normal as showed in [Table 2]. The changes of blood glucose before and after surgery are shown in [Table 2], too. Among them, two cases were found to have a delayed wound healing. In accordance with the diagnostic criteria for postoperative pancreatic fistula set by International pancreatic fistula study group in 2005, we found that in this group of patients, we found that in this group of patients, there were three patients with pancreatic fistula, of which A, B, and C grade were one patient each, respectively. Therefore, the total occurrence ratio of pancreatic fistula was 17.6% (3/17). Treatment of pancreatic fistula: To keep the abdominal cavity drainage unobstructed, discharging with tube was recommended. Among them, two cases were healed spontaneously within 2 months postoperatively, one case healed within 5 months postoperatively. Mild to moderate diarrhea (watery stool) occurred in three patients 1–2 weeks postoperatively, by which the trypsin treatment was administrated for 1–2 weeks to alleviate the symptoms. The incidence of diarrhea was 17.6% (3/17). The total complication rate was 47.1% (8/17).
Table 2: Changes of biochemical indexes before and after operation

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Recent efficiency

Abdominal pain and back pain were significantly improved in all patients after 1 week of operation, and the VAS score was significantly decreased (P < 0.05) compared with the before [Table 1]. Compared with preoperative, the average weight was 4.1 ± 1.3 kg (95% CI: 1.3 kg ~6.9 kg, t = 3.127, P = 0.007) higher than 6 weeks after surgery, with an average increase of 6.4%. The scores of quality of life were significantly improved (P < 0.05) [Table 1].


During the follow-up period (3–60 months, average 19.0 ± 3.5 months, median follow-up time 16 months), all patients were followed up effectively. During the follow-up period, one patient received palliative resection and two patients received local radiotherapy. The other patients received chemotherapy, but they were died 5 and 9 months after surgery for tumor recurrence and progression. Of the 15 cases with R0 resection, 8 cases had recurrence and metastasis, 1 case had extensive metastases, 5 cases with liver metastasis, 1 case with pulmonary metastasis, and 1 case with abdominal metastasis and liver metastasis. Patients with single liver metastasis or lung metastasis were treated with radiofrequency ablation after reaching agreement with the patients themselves and their families. Besides, three included cases were treated with adjuvant chemotherapy. In addition, no cases of primary resection or residual tumor recurrence were found during the follow-up period. The 1-, 2-, 3- and 5-year recurrence rates of patients were 22.9%, 58.9%, 72.6%, and 72.6%, respectively. As shown in [Figure 1], the median recurrence and metastasis time of patients was 20.0 ± 3.8 months (95% CI: 12.6–27.4 months). Eight patients died during the follow-up period, allowing to tumor progression, recurrence, and metastasis. The 1-, 2-, 3- and 5-year survival rates of patients were 80.4%, 54.2%, 32.5% and 16.3%, respectively. The median survival time was 26.0 ± 6.0 months (95% CI: 14.2–37.8 months) [Figure 2].
Figure 2: Postoperative survival rate

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 > Discussion Top

The advantage of improved Appleby operation is that the reconstruction of vascular anastomosis is not necessary, which reduces the difficulty of traditional Appleby surgery. The anatomical basis of this technique is as follows: The hepatic blood flow can be separated to the arteriae gastroduodenalis through the bypass constructed by superior mesenteric artery pancreatic and duodenal vascular arch. Finally, hepatic blood flow can be reversed into the hepatic artery through the gastroduodenal artery. Anatomic study had confirmed the presence of this bypass. Therefore, the gastric and duodenal arteries become the main source of blood supply of liver and stomach after received Appleby.[10],[11] What's more, it was considered as an essential way to ensure the blood supply of the liver and stomach to reduce the incidence of ischemic complications.[12]

As to the incidence of mortality and complications associated with Appleby surgery, Sperti et al. showed that the mortality and incidence were 2.1% and 40.6% respectively, while Kondo et al. concluded that it was 0% and 62%.[13],[14] The data of the present study were consistent with the previous reports. The results showed that the postoperative mortality was 0%, the total incidence of complication was 47.1%, which mainly consist of pancreatic leakage and diarrhea. However, the complication of liver abscess, gallbladder necrosis, gastric ulcer, gastrointestinal bleeding was not evident. One day after surgery, ALT, AST, and other liver function indicators can be significantly increased, but then decreased, and the indexes mentioned above recovered to the normal level 1 week after surgery. However, we also found that there was no significant increase in blood glucose in patients after surgery. This suggests that Appleby is safe and effective in the treatment of pancreatic body and tail carcinoma. Due to the anatomical location of the body of the pancreas is deep, when the carcinoma of the pancreatic body and tail was diagnosed, most of the peripheral blood vessels have been infiltrated by the tumor tissue, even nerve plexus. Furthermore, the intractable abdominal pain occurs and finally affect the quality of life of patients. The celiac trunk and hepatic artery, which have been infiltrated by tumor, can be removed by Appleby surgery. The infiltration of the retroperitoneal nerve plexus together with the tumor was removed by this way. In the present study, most cases achieved a complete remission in abdominal pain after Appleby surgery. Besides, weight gain and an improvement of quality of life can be also observed significantly.

According to the report of Nordback et al., the resection rate of nonAppleby in patients with pancreatic body and tail carcinoma was 10%, and the postoperative survival rate within a single year was about 8–9% with an average survival time of 3–4 months.[15] The main reason for the poor prognosis of the pancreatic body and tail carcinoma is that most of the major vessels of the pancreas have been invaded by the tumor, and thus lose the best opportunity to surgery. Therefore, it is possible to improve the surgical resection rate of pancreatic body and tail carcinoma by Appleby surgery to improve the survival rate. Hirano et al. reported that a survival rate of 1 and 5 years of patients with pancreatic body and tail carcinoma after Appleby operation, was as high as 71% and 42%, respectively.[16] Moreover, the median survival time was 21 months. In the present study, the corresponding data were 80.4%, 16.3%, and 26 months. In addition, the data also showed that the main cause of death in patients with Appleby after surgery is the recurrence and metastasis of cancer. The recurrence and metastasis rate of patients after 1, 2, 3, and 5 years were 22.9%, 58.9%, 72.6%, 72.6%, respectively, and the prediction of recurrence and metastasis was 20 months, which indicates that although Appleby has improved the resection rate of pancreatic body and tail carcinoma, the recurrence is still higher and earlier, which become a major factor affecting the survival rate of patients generally. Therefore, the use of postoperative adjuvant chemotherapy may be helpful to improve the postoperative survival rate and prolong the survival time of patients.[16] However, this conclusion still needs to be further confirmed through theoretical study.

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Conflicts of interest

There are no conflicts of interest.

 > References Top

Nimura Y, Hattori T, Miura K, Nakajima N, Hibi M. Experience of Appleby's operation for advanced carcinoma of the pancreatic body and tail. Shujutsu 1976;30:885-9.  Back to cited text no. 1
Cartwright T, Richards DA, Boehm KA. Cancer of the pancreas: Are we making progress? A review of studies in the US Oncology Research Network. Cancer Control 2008;15:308-13.  Back to cited text no. 2
Hishinuma S, Ogata Y, Matsui J, Ozawa I, Inada T, Shimizu H. Two cases of cancer of the pancreatic body undergoing gastric preservation with distal pancreatectomy combined with resection of the celiac axis. Jpn J Gastroenterol Surg 1991;24:2782-6.  Back to cited text no. 3
Shoup M, Brennan MF, McWhite K, Leung DH, Klimstra D, Conlon KC. The value of splenic preservation with distal pancreatectomy. Arch Surg 2002;137:164-8.  Back to cited text no. 4
Baumgartner JM, Krasinskas A, Daouadi M, Zureikat A, Marsh W, Lee K, et al. Distal pancreatectomy with en bloc celiac axis resection for locally advanced pancreatic adenocarcinoma following neoadjuvant therapy. J Gastrointest Surg 2012;16:1152-9.  Back to cited text no. 5
Vadalà S, Aronica G, Biondi A, Magnano V, Valastro M, Li Volti G, et al. Distal pancreatectomy with en bloc resection of the celiac axis for pancreatic adenocarcinoma. Clin Ter 2009;160:287-90.  Back to cited text no. 6
Baumgartner JM, Krasinskas A, Daouadi M, Zureikat A, Marsh W, Lee K, et al. Distal pancreatectomy with en bloc celiac axis resection for locally advanced pancreatic adenocarcinoma following neoadjuvant therapy. J Gastrointest Surg 2012;16:1152-9.  Back to cited text no. 7
Grützmann R, Distler M, Weitz J. Appleby operation for locally advanced tumour of the pancreatic body and tail – A video demonstration. Zentralbl Chir 2015;140:151-4.  Back to cited text no. 8
Collins SL, Moore RA, McQuay HJ. The visual analogue pain intensity scale: What is moderate pain in millimetres? Pain 1997;72:95-7.  Back to cited text no. 9
Eypasch E, Williams JI, Wood-Dauphinee S, Ure BM, Schmülling C, Neugebauer E, et al. Gastrointestinal quality of life index: Development, validation and application of a new instrument. Br J Surg 1995;82:216-22.  Back to cited text no. 10
Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, et al. Postoperative pancreatic fistula: An international study group (ISGPF) definition. Surgery 2005;138:8-13.  Back to cited text no. 11
Wang X, Dong Y, Jin J, Liu Q, Zhan Q, Chen H, et al. Efficacy of modified Appleby surgery: A benefit for elderly patients? J Surg Res 2015;194:83-90.  Back to cited text no. 12
Sperti C, Berselli M, Pedrazzoli S. Distal pancreatectomy for body-tail pancreatic cancer: Is there a role for celiac axis resection? Pancreatology 2010;10:491-8.  Back to cited text no. 13
Kondo S, Katoh H, Hirano S, Ambo Y, Tanaka E, Okushiba S, et al. Results of radical distal pancreatectomy with en bloc resection of the celiac artery for locally advanced cancer of the pancreatic body. Langenbecks Arch Surg 2003;388:101-6.  Back to cited text no. 14
Nordback IH, Hruban RH, Boitnott JK, Pitt HA, Cameron JL. Carcinoma of the body and tail of the pancreas. Am J Surg 1992;164:26-31.  Back to cited text no. 15
Hirano S, Kondo S, Tanaka E, Shichinohe T, Tsuchikawa T, Kato K, et al. Postoperative bowel function and nutritional status following distal pancreatectomy with en-bloc celiac axis resection. Dig Surg 2010;27:212-6.  Back to cited text no. 16


  [Figure 1], [Figure 2]

  [Table 1], [Table 2]


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