ORIGINAL ARTICLE

Characteristics of Pancreaticoduodenal Resection

on Periampullary Tumor Cases by Jakarta
Tertiary Hospital Team: Three Decade Report
Toar JM Lalisang*, Yarman Mazni*, Yefta Moenadjad*, Sahat Matondang**
*Department of Surgery, Faculty of Medicine, Universitas Indonesia/
Dr. Cipto Mangunkusumo General National Hospital, Jakarta
**Department of Radiology, Faculty of Medicine, Universitas Indonesia/
Dr. Cipto Mangunkusumo General National Hospital, Jakarta

Corresponding author:
Toar JM Lalisang. Department of Surgery, Dr. Cipto Mangunkusumo General National Hospital. Jl. Diponegoro
No. 71 Jakarta Indonesia. Phone/facsimile: +62-21-3148705. E-mail: [email protected]

ABSTRACT

Background: There were only few publications related to pancreaticoduodenal resection (PDR) /Whipple
procedure in Indonesia in the past decade.
Method: Retrospectively report of the characteristics and outcomes of PDR performed by Cipto Mangunkusumo
Hospital surgical team from 1993 to 2017 were collected.
Results: PDR were performed in 213 patients, with a mean age of 50.6 years and 54.4% patients were females.
Predominant preoperative clinical findings were jaundice (68.9%) and mild hypoalbuminemia (69.9%). Biliary
decompression was performed in 112 (52.6%) subjects. Average surgical waiting time was 3.5 months. While PDR
were performed in 84 (39.5%) subjects, pyloric preserving pancreaticoduodenal technique was predominated
in 128 (59.8) and predominated, especially during the latter years. Fifteen (9.0%) cases were benign. Thirty-
one (14.6%) subjects underwent relaparotomy, 16 (51.6%) of whom died post-operatively. Overall operative
mortality decreased from 16.9% to 5.5% in 2016, while resection rate generally increased over time, ranging from
2 - 21/year. Less than 10% of subjects survived for > 5 years, while < 20% survived for < 24 months. Overall
morbidity was 65.1% in 177 survivors, with surgical site infection in 52.5%, pancreatic fistula in 24.2%, and
post-pancreatectomy haemorrhage (PPH) as a fatal postoperative complication in 19 (8.9%) cases. Patients
who died within 30 days postoperatively had significantly more relaparotomies and PPH (p < 0.001).
Conclusion: Prolonged jaundice and mild hypoalbuminemia are dominant characteristics in our Indonesian
PDR subjects. Cipto Mangunkusumo Hospital is a high-volume PDR centre and world class hospital. Mortality
rates decreased with the increasing resection rates. Relaparotomy and PPH are predictors of poor outcome.

Keywords: hypoalbuminemia, prolonged jaundice, whipple.

ABSTRAK

Latar belakang: Tidak banyak publikasi terkait reseksi pankreaoduodenal/prosedur Whipple di Indonesia
pada dekade terakhir.
Metode: Penelitian dilakukan secara retrospektif menggunakan data prosedur Whipple yang dilakukan oleh
tim bedah Rumah Sakit Dr. Cipto Mangunkusumo dari 1993 hingga 2017.
Hasil: Prosedur Whipple dilakukan pada 213 subjek dengan rerata usia 50,6 tahun dan 54,4% di antaranya
perempuan. Temuan klinis preoperatif dominan yang didapatkan adalah ikterus dan hypoalbuminemia ringan.

66 The Indonesian Journal of Gastroenterology, Hepatology and Digestive Endoscopy

 Characteristics of Pancreaticoduodenal Resection on Periampullary Tumor Cases by Jakarta Tertiary Hospital Team: Three Decade Report

Dekompresi bilier dilakukan pada 112 (52,6%) subjek. Rerata waktu tunggu operasi adalah 3,5 bulan.
Reseksi dilakukan pada 84 (39,5%) subjek, pada 128 (59,8%) subjek dilakukan teknik pyloric preserving
pancreaticoduodenal. Sebanyak 15 (9,0%) kasus merupakan kasus jinak. Dari 31 (14,6%) pasien yang menjalani
relaparotomi, 16 (51,6%) di antaranya meninggal pascaoperasi. Mortalitas operasi menurun dari 16,9% ke
5,5% pada tahun 2016 sementara frekuensi reseksi semakin meningkat, antara 2-21 per tahun. Kurang dari 10%
subjek bertahan hidup > 5 tahun sementara < 20% subjek bertahan < 24 bulan. Morbiditas didapatkan sebesar
65,1% dari 177 subjek dengan infeksi daerah operasi sebanyak 52,5%, fistula pankreas 24,2% dan perdarahan
pascapankreatektomi 19 (8,9%) subjek. Relaparotomi dan perdarahan pascapankreatektomi jumlahnya signifikan
pada subjek yang meninggal < 30 hari pasca operasi (p < 0,001)
Simpulan: Ikterus berkepanjangan dan hipoalbuminemia merupakan karakteristik dominan subjek dengan
reseksi pankreatoduodenal di Indonesia. Rumah Sakit Dr. Cipto Mangunkusumo merupakan pusat reseksi
pankreatoduodenal dengan frekuensi tindakan yang tinggi. Terdapat hubungan antara jumlah reseksi dengan
mortalitas. Relaparotomi dan perdarahan pascapankreatektomi merupakan prediktor luaran buruk pada subjek.

Kata kunci: hipoalbuminemia, ikterus berkepanjangan, whipple.

INTRODUCTION were divided into 3 periods of time. The PDR data

of the first period, which was from 1993-2003, was
Indonesia has the largest national population in the
published descriptively in 2004.4 The second period,
east equator, but no study about pancreatico-duodenal
between 2004 and 2010, was specified due to almost
and pyloric preserving pancreaticoduodenal resections
all dissection, resection, and pancreaticojejunostomy
has been published in the last 10 years, compared to
anastomosis was performed by the authors themselves.
reports coming from other South East Asia countries.1–6
In the last period, 2011 until December 31st 2017, there
In fact, the volume of resection or hospital load
were 3 surgeons who performed the operation.
to pancreaticoduodenal (PD)/pylorus-preserving
Subject characteristics, perioperative work–up,
pancreaticoduodenectomy (PPPD) in South East Asia
procedure of resection, and histopathological findings
region, even from hepatopancreaticobiliary (HPB)
were the variables of interest and were analysed. Data
leading centres, were low.1–7
was presented in mean, standard deviation, or range.
Pancreaticoduodenal resection is the only treatment
Morbidity was defined as it was already written in
of choice shown to contribute to prolonged-survival,
other journal before.4 Operative mortality was defined
even though the risk of major complications is around
as death occurring up to 30 days after the operation
57%.8,910 Morbidity and survival rate of operable and
or during hospitalization. Kaplan–Meier analysis
resectable malignant peri–ampullary tumors (PT)
was used in the evaluation of overall survival and
remain a challenge in the field of surgery, although the
malignancy survival based on staging.
operative mortality was less than 4% in HPB surgery
centres since the last millenium.7,8,11–14
A high success rate of complex high–risk tertiary RESULTS
surgical procedures for malignant PT indicates the quality
Two hundred and thirteen resection procedures were
of surgical care in a world class hospital and an excellent
documented. Demographic characteristics, laboratory
medical center.12,14,15 Surgical skills and experiences
preoperative and perioperative data, resection type,
contribute to outcomes, in addition to perioperative
and complications of the operation are described in
assessment and support.7,10,12,16 This paper reviewed the
3 periods of time in Table 1. Jaundice was the most
characteristic and the outcome of the PD/PPPD resection.
common clinical finding in 147 (68%) procedures
followed by abdominal pain, while nausea, vomiting,
METHOD abdominal mass, and melena were minor findings.
The average pre-hospital symptom duration was 2.6
Retrospective reports of patients who were
months, with a month of preoperative work–up.
preoperatively diagnosed with PT were collected
Routine abdominal ultrasounds were done in all
from 1993 until 2017. These patients underwent PD or
patients at initial workups. Later, diagnostic workups
PPPD resection and total pancreatectomy (TP). Data
included standardized abdominal contrast-enhanced

Volume 20, Number 2, August 2019 67

 Aspiration 0 2 (1.7) 0 (0) 2
Operative time (minutes) 427.9 428 449.5 439.5
Operative mortality 8 (22,2%) 16 (19.7%) 12 (12.6%) 36 (16.9%)
Length of stay (days) 22.1 18.2 14.2 17.6
Toar JM Lalisang, Yarman Mazni, Yefta Moenadjad, Sahat Matondang
Annual resection rate and operative mortality based on 3 period times were presented
in Figure 1. Overall operative mortality was 16.9%, consisting of 22 males and 14 females,
which fluctuated, with a range of 1–5 deaths annually. No mortality occurred in 2000, 2004,
computed scan. During the last 10 years, magnetic (LOS) ranged from 9-32 days, with an overall mean
2007, and 2011. Operative mortality decreased to nearly half in the last period and compared
resonance imaging (MRI)/magnetic resonance of 17.6+8.7 days. In the last 3 years, the average LOS
to the first period dropped to 5.5% in 2016. The highest annual resection procedure was 21 in
cholangiopancreatography (MRCP) was performed decreased to 12.9 days.
2014, and PPPD was more common after 2005. Primary total pancreatectomy (TP) was
for diagnostic and resectability confirmation. Pathologically,
performed in two subjects with198 (92.9%)
pancreatic malignancies
head malignancy were6 months
whom died within
Mismatches in preoperative imaging interpretation documented,
postoperatively, consisting
suffering of stagesdueI,to apancreatic
from severe hypoglycaemia II, III, diabetes.
and IV Another TP

and intraoperative finding were found in around 30% of (20.4%, 47.6%, 30.7%, and 1.8%, respectively. days
was indicated to treat anastomotic leakage at relaparotomy. The patient died several
postoperatively. Postoperative length of stay (LOS) ranged from 9-32 days, with an overall
subjects (64 cases), due to the time lag from radiologic Adenocarcinoma was found in 187 (94.7%) subjects.
mean of 17.6+8.7 days. In the last 3 years, the average LOS decreased to 12.9 days.
examination to the operative procedure with an average Carcinoma of ampulla of Vater and pancreatic head
Pathologically, 198 (92.9%) malignancies were documented, consisting of stages I, II,
of 3.5 months. cases were mostly
III, and IV (20.4%, 47.6%, 30.7%,in stages I and
and 1.8%, II, while
respectively. subjectswas
Adenocarcinoma with
found in 187
Annual resection rate and operative mortality carcinoma
(94.7%) subjects. of duodenum
Carcinoma of ampulla(25 subjects)
of Vater were
and pancreatic headmostly
cases wereinmostly in
based on 3 period times were presented in Figure 1. stages
stages I andII andsubjects
II, while III. All
with stage
carcinomaIV subjects
of duodenum (25 were
subjects)found toin stages
were mostly

Overall operative mortality was 16.9%, consisting have carcinoma of the pancreatic head post-operatively.
II and III. All stage IV subjects were found to have carcinoma of the pancreatic head post-
operatively.
of 22 males and 14 females, which fluctuated,
PDR Volume and Operative Mortality
with a range of 1–5 deaths annually. No mortality .
occurred in 2000, 2004, 2007, and 2011. Operative 25

mortality decreased to nearly half in the last period 20

and compared to the first period dropped to 5.5% in 15

2016. The highest annual resection procedure was 21 10

in 2014, and PPPD was more common after 2005. 5

Primary total pancreatectomy (TP) was performed in 0

two subjects with pancreatic head malignancy whom

1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2 010 2011 2012 2013 2014 2015 2016 2017

Resection Volume Operative Mortality

died within 6 months postoperatively, suffering from Figure 1. Resection rate and operative mortality in 1993-2017
Figure 1. Resection rate and operative mortality in 1993-2017
severe hypoglycaemia due to apancreatic diabetes.
Another TP was indicated to treat anastomotic Gastrointestinal stromal tumour (GIST),
leakage at relaparotomy. The patient died several neuroendocrine tumour, squamous cell carcinoma,
days postoperatively. Postoperative length of stay and malignant lymphoma were found in 2 (1.01%)

Table 1. Demography, perioperative, surgery technique and output data presented mean in 3 periods of time
Year Period 1993-2003 2004- 2010 2011-2017 Total
n resection 37 81 95 213
Gender
Female 22 34 55 111
Male 15 47 40 102
Age (year) 45.2 52.1 54.2 50.6
Hemoglobin (g/dL) 11.1 11.3 11.4 11. 3
Hematocrit (%) 31.2 33.8 33.5 30.4
White blood count (/µL) 10778 11436 9570 11346
Albumin (g/dL) 3.3 3.36 3.30 3.32
Bilirubin (mg/dL) 8.6 7.11 3.56 6.2
Alkaline phosphate (U/L) 859 532 242 530
Ureum (mg/dL) 31.2 31.7 22 29.4
Creatinine (mg/dL) 0.56 0.7 0.7 0.62
Resection types
pylorus-preserving pancreaticoduodenecto-
my (PPPD) 14 63 51 128
Whipple 21 18 44 84
Total pancreatectomy (TP) 2 0 0 2
Intra-operative blood loss
1111.2 733.8 834 677
(mean in cc)
Re-laparotomy 7 (18.9%) 14 (17.2%) 10 (10.6%) 31 (14.5%)
Surgical site infection 12 (29.7%) 28 (34.5%) 17 (17.9%) 57 (26.7%)
Pneumonia 1 5 (5.1%) 0 (0) 6
Pancreatic fistula 0 11 16 27
Delayed gastric emptying 2 12 (14.8%) 10 (10.6%) 24
Post pancreatic hemorrhage (PPH) 0 8 (6.8) 11 (5.8) 19
Aspiration 0 2 (1.7) 0 (0) 2
Operative time (minutes) 427.9 428 449.5 439.5
Operative mortality 8 (22,2%) 16 (19.7%) 12 (12.6%) 36 (16.9%)
Length of stay (days) 22.1 18.2 14.2 17.6

68 The Indonesian Journal of Gastroenterology, Hepatology and Digestive Endoscopy

 Characteristics of Pancreaticoduodenal Resection on Periampullary Tumor Cases by Jakarta Tertiary Hospital Team: Three Decade Report

Table 2. Preoperative diagnosis and final pathological result

Preoperative diagnosis n (%) Histopathology n (%) Stage I/II/III/IV n (%)
Pancreatic head tumour 64(30) Carcinoma of pancreatic head 70(33) 9/28/25/3 65(37)
Papilla/ampullasubject with colon
of Vater tumour metastasis
71(33.3) survived
Carcinoma up toampulla
of papilla/ 10 years. The91(43)
of Vater overall 5 years survival of83(47)
21/42/20/0 all PT
Distal common bile duct (CBD) 15(7) Carcinoma of distal common bile duct 3(1.4) 3/ 0/ 0/ 0 3 (1.7)
tumour cases, based on stage and histopathology
(CBD) were shown on Kaplan Meier curves in Figure 2 and
Tumour of the duodenum 16(7.5) Tumour of duodenum 25(12) 3/12/10/ 0 25(14.3)
3.
Periampullary tumour 22(10.3) peri-ampullary tumors (PT) non– 11(4,2)
adenocarcinoma*   
Others 14(6.6) Benign tumors 15(9.5)
*Signet ring cell; neuroendocrine tumour, GIST; malignant lymphoma

subject with colon metastasis

l survived up to 10 years. The ov
cases, based on stage and histopathology were shown on Kapla
3.

Figure 2. Kaplan Meier curve of periampullary malignancy overall survival (left) and survival of
Figure 2. Kaplan
periampullary Meier based
malignancy curveon ofstadium
periampullary
(right) malignancy overall survival (left) and survival
of periampullary malignancy based on stadium (right)
subjects each; One subject had metastasis of colonic (7.34%) survived for more than 5 years. We estimated
adenocarcinoma on the pancreatic head who was alive that an additional 16 (surgery in 2014 or after) subjects
without disease until the data were reviewed. Signet who have not yet surpassed the 5-year period will
ring cell carcinoma was seen in 2 (1.01%) duodenal bring the total to 29 (16.4) subjects. Two subjects with
tumour subjects. primary periampullary malignancy and one subject
Discrepancies between preoperative diagnosis with colon metastasis survived up to 10 years. The
and final pathologic result were noted in 9-22% of overall 5 years survival of all PT cases, based on stage
pancreas and Vater malignant cases in detailed showed and histopathology were shown on Kaplan Meier
in Table 2. Most of the benign cases were confirmed curves in Figure 2 and 3.
after operation. The 5 years overall survival for all PT cases were
Morbidity was noted in 177 (83.1%) survivors; Figurewith
15.1% 2. Kaplan Meier
a median of curve
19 (95%of periampullary malignancy ov
CI: 13-24) months.
31 (14.5%) re–laparotomies were documented, due of periampullary malignancy based on stadium
The 5 years survivor of all cases, excluding the (right)
to inadequate drainage of pancreaticobiliary leakage, operative mortality was 13.8%. Median survival was
leading to abdominal sepsis, bowel transit problems,
worsening organ dysfunction, and bleeding post-
pancreatectomy
Figurehaemorrhage
3. Kaplan-Meier (PPH).
curveThe worst
of pancreatic ductal adenocarcinoma (PDAC), ampulla vateri
documentedadenocarcinoma
complications leading to operative
(AVAC) and duodenal adenocarcinoma (DAC)
mortality were abdominal sepsis (10 subjects), multiple
organ failure (10 subjects), and post-pancreatectomy
The 5 years
haemorrhage (14 subjects). overallpneumonia
Aspiration survival forinall PT cases were 15.1% with a median of 19 (95% CI:
two delayed13-24)
gastricmonths.
emptyingThe(DGE)
5 yearssubjects
survivorwas of all cases, excluding the operative mortality was 13.8%.
noted to be a lethal complication.
Median survival was 17 (95% CI: 0.8-23) months. The malignancy cases over all 5 years
Post-pancreatectomy haemorrhage (PPH) and
survival was
aspiration pneumonia 18%, with
contributed a median
to early of 15 (95% CI: 10-19.8) months. The 5 years survival of
operative
mortality (7-10
PDAC,days),
AVACwhileand
abdominal
DAC were sepsis and
11.7%,31,8% and 14.3% respectively. Based on staging, the 5
multiorgan failure (MOF) contributed to late operative
yearsdays),
mortality (10-42 survival of occurred
which stage I, in
II, 5and III were 10%, 18% and 9.09% respectively. The median
cases.
Among the survivors, 130 patients (73.5%) had Figure 3. Kaplan-Meier curve of pancreatic ductal
Figure 3. Kaplan-Meier curve vateri
of pancreatic ductal adenocar
adenocarcinoma (PDAC), ampulla adenocarcinoma
died when this review was made, Overall, 13 subjects adenocarcinoma
(AVAC) (AVAC) and duodenal
and duodenal adenocarcinoma (DAC) adenocarcinoma (DA

Volume 20, Number 2, August 2019 69 were 15.1%

The 5 years overall survival for all PT cases
13-24) months. The 5 years survivor of all cases, excluding the
Toar JM Lalisang, Yarman Mazni, Yefta Moenadjad, Sahat Matondang

17 (95% CI: 0.8-23) months. The malignancy cases after resection, with patients mostly presenting with
over all 5 years survival was 18%, with a median of chronic jaundice and malnutrition 12,25 In addition,
15 (95% CI: 10-19.8) months. The 5 years survival 68% of perioperative infection was documented in
of PDAC, AVAC and DAC were 11.7%,31,8% and those with serum albumin < 3.0 mg/dL. Reduced
14.3% respectively. Based on staging, the 5 years total bilirubin showed better outcomes, similar to past
survival of stage I, II, and III were 10%, 18% and reports.26.27,28 Furthermore, hospital delay is another
9.09% respectively. The median survival period for characteristic which may endanger patients in this
periampullary malignancy stage I was 24 (95% CI: region. During the time lag, their condition may
00-49) months, stage II 12 (95% CI: 4.1-19) months convert from a resectable to an un-resectable, or even
and stage III was 12 (95% CI: 5.6-18.3) months. Three inoperable case. Preoperative work–ups and referral
stage IV cases died less than 6 months after surgery. waiting lists were the most common causes of delay.
The TP procedure is no longer used by our
surgical team due to difficulty in management of
DISCUSSION
post-operative apancreatic diabetes. Moreover, other
This study reported the characteristics and studies also concluded that the procedure has many
outcomes of PD resections in the management of disadvantages.10,29 The reconstruction technique was
periampullary tumour performed by a single surgical done with the single jejunal loop protocol, which is side–
team from the main referral hospital in Indonesia, to–end pancreaticojejunostomy in combination with
over a 24-year period. The timeline was divided into duct–to–enteral in complement of Dunking technique;
3 periods based on specific conditions. Operative Hence, the combination was named the entero–
mortality in 2016 reached its nadir of 5.5%, which Dunking technique. As such, there was no tension on
was similar to other medical centres worldwide.7–9,12 the anastomosis, and the jejunal diameter could easily
This progress was related to the gradual increase of be adjusted to the pancreatic stump, providing good
resection volume over the years, reaching an averages drainage to the distal segment by autoperistalsis.30 In
of 13.6 procedures annually which accounts it as a a dealing with pancreatico–jejunostomy anastomosis
high volume PDR centre.1,5,8,16 A recent study set 40 PD failure, the pancreatic stump including the duct were
resection procedures threshold as a predictive factor tied up, then the jejunostomy was closed.19 
for better outcome.17 In the early years until mid-2000, Malignant periampullary tumor, postoperative
operative mortality was 2–3 times higher than the histopathological finding, and staging were also in line
leading centre. This finding was related to insufficient with those in past reports, with predominantly stage I and
preoperative work–up, infection control, a routine II.7,12,18,21,31 An exception was a subject in stage IV who
standard operational procedures, and the learning underwent resection, as the criteria of resectability was
curve.16,13,17,18 Higher resection volume multiplies the met and the metastasis was confirmed retrospectively.
surgeon’s experience, generating better results even in Primary GIST and signet ring cell of the duodenum were
low volume hospitals notably rare pathologies.9 All morbidities found were
High operative mortality in this report was associated quite high compared to prior reports, but the destructive
with re–laparotomy procedures, which were performed problems could be managed well.12,23
when indicated due to PPH, sepsis, and multiple organ All types of actual pancreatic fistulation in our cases
failure. More than 44.9% of subjects with re–laparotomy (24.2%) consisted of pancreatic leaks manifesting as
died postoperatively, which was high compared to abdominal sepsis and GI bleeding. Forty percent of
other published reports.19,20 The incidence increased the type A or B pancreatic leaks healed spontaneously
mostly due to gastroduodenal artery injury secondary due to good drainage, and was, notably, three times
to pancreatic leak. Bleeding and sepsis following higher compared to the previously published reports
anastomosis leakage of the pancreaticojejunostomy (7% in a leading centre).7,11,12,21,30,31 DGE (10.9%)
indicates inadequate drainage.21,22 Aspiration occurred was higher than in the past reports and was found
in two subjects with DGE, due to the early removal of in both classical Whipple and PPPD.14,32,33,34 All
the decompression tube, while active production was remaining patients were successfully managed with
ongoing. Aspiration was a sentinel event and contributed intermittent gastric decompression, early oral solid
to operative mortality.23,24 enteral feeding in a small–frequent scheme, in addition
Delayed presentation contributed to a narrow to oral erythromycin suspension as well as early
spectrum of safety margin for a successful recovery mobilization.

70 The Indonesian Journal of Gastroenterology, Hepatology and Digestive Endoscopy

 Characteristics of Pancreaticoduodenal Resection on Periampullary Tumor Cases by Jakarta Tertiary Hospital Team: Three Decade Report

Length of postoperative stay in the study reduced surgery for periampullary tumors: a comparison of
from 17.6 to 12.9 days in the last 5 years, in parallel short-term clinical outcomes of laparoscopy-assisted
pancreaticoduodenectomy and open pancreaticoduodenectomy.
with the application of fast tract recovery systems J Hepatobiliary Pancreat Sci 2015;22:819-24.
and better perioperative preparation.11,12,35 Survival 3. Norsa’ AB, Nur-Zafira A, Knight A. Pancreatic cancer in
was difficult to be accurately evaluated, as loss of Universiti Sains Malaysia hospital: a retrospective review of
follow up after 1 year was quite high (30%). However, years 2001-2008. Asian Pac J Cancer Prev 2012;13:2857-60.
Kaplan–Meier analysis showed that survival rate based 4. Lalisang TJM, Simanjuntak A, Philippi B.
Pancreaticoduodenectomy for periampullary tumors at Dr.
on the stage of tumour was less than those reported.16,36 Cipto Mangunkusumo Hospital, Jakarta. Med J Indones
The analysis and direct actual counting showed a 5% 2004;13:166-70.
discrepancy in the 5-year survival rates. Objectively, 5. Khaimook A, Bokird J, Alapach S. Case report the first
survival in stage II resected subjects was better successful laparoscopic whipple procedure at Hat Yai
Hospital: surgical technique and a case report. J Med Assoc
compared to non–operated patients, who survived less Thai 2010;93:1098-102.
than 18 months.37 In those who survived less than 1 6. Boonnuch W, Akaraviputh T, Lohsiriwat D. Whipple’s
year (particularly in 6 months), considering the period operation without an operative mortality in 37 consecutive
of sickness, we found that the subjects survived in patients: Thai surgeons’ experiences. J Med Assoc Thai
2005;88:467-72.
3 months with a condition that was not necessarily
7. Shrikhande SV, Barreto SG, Somashekar BA, Suradkar K,
disease–free. Shetty GS, Talole S, et al. Evolution of pancreatoduodenectomy
Finally, our data shows that Cipto Mangunkusumo in a tertiary cancer center in India: improved results from
Hospital has applied the mobile team approach, service reconfiguration. Pancreatology 2013;13:63-71.
supported by multidisciplinary involvement, in a well– 8. Tani M, Kawai M, Hirono S, Ina S, Miyazawa M, Nishioka
R, et al. A pancreaticoduodenectomy is acceptable for
organized fashion. Achievements in resection volume periampullary tumors in the elderly, even in patients over 80
and mortality rate showed improvements equal to world years of age. J Hepatobiliary Pancreat Surg 2009;16:675-80.
class medical centres, although the outcomes remain 9. Yamaue H, Tani M, Kawai M, Hirono S, Okada K,
varied. Any fluctuations of outcome, especially the Miyazawa M. Pancreatic dissection in the procedure of
pancreaticoduodenectomy (with videos). J Hepatobiliary
operative mortality, was related to the characteristics in Pancreat Sci 2012;19:95-9.
the region, i.e., advanced cases, obstacles in scheduling 10. Bressan AK, Wahba M, Dixon E, Ball CG. Completion
a resection, variation of stage, and chronicity of the pancreatectomy in the acute management of pancreatic
disease itself, all of which tend to narrow the spectrum fistula after pancreaticoduodenectomy: a systematic review
and qualitative synthesis of the literature. HPB Oxford
of tolerance to complications. We learned that cases 2018;20:20-7.
should be carefully selected with zero compromise 11. Schmidt CM, Turrini O, Parikh P, House MG, Zyromski
for error in the preoperative setting, in order to ensure MJ, Nakeeb A, et al. Effect of hospital volume, surgeon
success. Thus, adequate and safe surgery should be the experience, and surgeon volume on patient outcomes after
pancreaticoduodenectomy: a single institution experience.
guiding principle for moving forward. The limitation of Arch Surg 2010;145:634-40.
this study was that we were unable to acquire complete 12. Cameron JL, Riall TS, Coleman J, Belcher KA. One
follow-up data for almost 30% of patients due to loss of thousand consecutive pancreaticoduodenectomies. Ann Surg
contact (20% subjects were referred from other regions 2006;244:10-5.
in the country). 13. Onete VG, Besselink MG, Salsbach CM. Impact of
centralization of pancreatoduodenectomy on reported radical
In conclusion, prolonged jaundice and resections rates in a nationwide pathology database. HPB
hypoalbuminemia are dominant characteristics, the (Oxford) 2015;17:736-42.
resection management of resectable PT has better 14. Malleo G, Vollmer CM. Postpancreatectomy complications
progress and is in line with other excellent centres. and management. Surg Clin North Am 2016;96:1313-36.
15. Birkmeyer JD, Siewers AE, Finlayson EV, et al. Hospital
Cipto Mangunkusumo Hospital is now a world class volume and surgical mortality in the United States. N Engl J
hospital and an excellent medical centre. Relaparotomy Med 2002;346:1128-37.
and PPH were predictors of poor outcomes. 16. Alsfasser G, Leicht H, Günster C, Rau BM, Schillinger G,
Klar E. Volume – outcome relationship in pancreatic surgery.
Br J Surg 2016;103:136-43.
REFERENCES 17. Van deer Gest LGM, van Rijssen LB, Molenaar IQ, de
Hingh IH, Groot Koerkamp B, Busch OR. Volume-outcome
1. Kwok KHK, Rizk J, Coleman M, Fenton-Lee D.
relationships in pancreatoduodenectomy for cancer. HPB
Pancreaticoduodenectomy-outcomes from an Australian
(Oxford) 2016;18:317-24.
institution. ANZ J Surg 2010;80:605-8.
18. Myatra S, Divatia JV, Jibhkate B, Barreto GS, Shrikhande SV.
2. Mendoza AS, Han H, Yoon YS, Cho JY, Choi Y. Laparoscopy-
Preoperative assessment and optimization in periampullary
assisted pancreaticoduodenectomy as minimally invasive
and pancreatic cancer. Indian J Cancer 2011;48:86-93.

Volume 20, Number 2, August 2019 71

Toar JM Lalisang, Yarman Mazni, Yefta Moenadjad, Sahat Matondang

19. Vijay A, Noaman I, Mahfouz A, Khawar M, Khalaf H, Elaffandi life after pancreatoduodenectomy with retrocolic or antecolic
A. Pancreatico-enteric fistula post pancreatic duct ligation for gastroenteric anastomosis. Br J Surg 2015;102:1123-32.
delayed haemorrhage complicating pancreaticoduodenectomy. 35. William sson C, Karlsson N, Sturesson C, Lindell G, Andersson
Int J Surg Case Rep 2016;21:29-31. R, Tingstedt B. Impact of a fast-track surgery programme for
20. Blanc T, Cortes A, Goere D, Sibert A, Pessaux P, Belghiti J, pancreaticoduodenectomy. Br J Surg 2015;102:1133-41.
et al. Hemorrhage after pancreaticoduodenectomy: when is 36. Karakatsanis A, Derpapas M, Chondroyannis A, Vezakis A.
surgery still indicated ? Am J Surg 2007;194:3-9. Prognostic factors for survival after pancreaticoduodenectomy
21. Kajiwara T, Sakamoto Y, Morofuji N, Nara S, Esaki M, for periampullary tumors. A single center experience.
Shimada K, et al. An analysis of risk factors for pancreatic Pancreatology 2012;12:557.
fistula after pancreaticoduodenectomy: clinical impact 37. Spanheimer PM, Cyr AR, Liao J, Johlin FC, Hoshi H, Howe
of bile juice infection on day 1. Langenbecks Arch Surg JR, et al. Complications and survival associated with operative
2010;395:707-12. procedures in patients with unresectable pancreatic head
22. Ansorge C, Nordin JZ, Lundell L, Strommer E, Rangelova adenocarcinoma. J Surg Oncol 2014;109:697-701.
J, Blomberg, et al. Diagnostic value of abdominal drainage
in individual risk assessment of pancreatic fistula following
pancreaticoduodenectomy. Br J Surg 2014;101:100-8.
23. Jilesen AP van Eijck CH, In't Hof KH, van Dieren S, Gouma
DJ, van Dijkum EJ. Postoperative complications, in-hospital
mortality and 5-year survival after surgical resection for
patients with a pancreatic neuroendocrine tumor: a systematic
review. World J Surg 2015;40:729-48.
24. Shubert CR, Kendrick ML, Thomsen KM, Farnell MB,
Habermann EB. Identification of risk categories for in
pancreaticoduodenectomy based on diagnosis. HPB (Oxford)
2015;17:428-37.
25. Fearon KC, Baracos VE. Cachexia in pancreatic cancer: new
treatment options and measures of success. HPB (Oxford)
2010;12:323-4.
26. Van der Gaag NA, Kloek JJ, de Castro SM, Busch OR,
van Gulik TN, Gouma DJ. Preoperative biliary drainage in
patients with obstructive jaundice: history and current status.
J Gastrointest Surg 2009;13:814-20.
27. Son JH, Kim J, Lee SH, Hwang JH, Ryu JK, Kim YT, et al.
The optimal duration of preoperative biliary drainage for
periampullary tumors that cause severe obstructive jaundice.
Am J Surg 2013;206:40-6.
28. Liu C, Lu JW, Du ZQ, Liu XM, Lv Y, Zhang XF. Association
of preoperative biliary drainage with postoperative morbidity
after pancreaticoduodenectomy. Gastroenterol Res Pract
2015;2015:796893.
29. Johnston WC, Hoen HM, Cassera MA, Newell PH, Hammill
CW, Hansen PD, et al. Total pancreatectomy for pancreatic
ductal adenocarcinoma: review of the National Cancer Data
Base. HPB (Oxford) 2016;18:21-8.
30. Shrikhande SV, Barreto G, Shukla P. Pancreatic fistula after
pancreaticoduodenectomy: the impact of a standardized
technique of pancreaticojejunostomy. Langenbecks Arch Surg
2008;393:87-91.
31. Kawai M, Tani M, Hirono S, Ina S, Miyazawa M, Yamaue
H. How do we predict the clinically relevant pancreatic
fistula after pancreaticoduodenectomy?— an analysis in 244
consecutive patients. World J Surg 2009;33:2670-8.
32. Huang W, Xiong JJ, Wan MH, Szatmary P, Bharucha
S, Gomatos I, et al. Meta-analysis of subtotal stomach-
preserving pancreaticoduodenectomy vs pylorus preserving
pancreaticoduodenectomy. World J Gastroenterol
2015;21:6361-73.
33. Walters DM, Shada AL, LaPar DJ, Adams RB, Bauer TW.
A long gastrojejunostomy is associated with decreased
incidence and severity of delayed gastric emptying after
pancreaticoduodenectomy. Pancreas 2015;44:1273-9.
34. Eshuis WJ, de Bree K, Sprangers MA, Bennink RJ, Van
Gulik TM, Busch OR, et al. Gastric emptying and quality of

72 The Indonesian Journal of Gastroenterology, Hepatology and Digestive Endoscopy