Intraoperative Transfusion is Independently Associated with a Worse Prognosis in Resected Pancreatic Cancer—a Retrospective Cohort Analysis
Abstract
:1. Background
2. Materials and Methods
3. Results
3.1. General Characteristics of the Patients
3.2. Chronological Trend and Potential Adverse Oncologic Impact of IOT
3.3. Determining Prognostic Factors in Resected Pancreatic Cancer
3.4. Predicting IOT in Resected Pancreatic Cancer
4. Discussion
Author Contributions
Funding
Conflicts of Interest
References
- Kamisawa, T.; Wood, L.D.; Itoi, T.; Takaori, K. Pancreatic cancer. Lancet 2016, 388, 73–85. [Google Scholar] [CrossRef]
- American Cancer Society, Cancer Facts & Figures 2020. Available online: https://www.cancer.org/research/cancer-facts-statistics/all-cancer-facts-figures/cancer-facts-figures-2020.html (accessed on 25 February 2020).
- Hidalgo, M. Pancreatic cancer. N. Engl. J. Med. 2010, 362, 1605–1617. [Google Scholar] [CrossRef] [Green Version]
- Asaoka, T.; Miyamoto, A.; Maeda, S.; Tsujie, M.; Hama, N.; Yamamoto, K.; Miyake, M.; Haraguchi, N.; Nishikawa, K.; Hirao, M.; et al. Prognostic impact of preoperative NLR and CA19-9 in pancreatic cancer. Pancreatology 2016, 16, 434–440. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, H.; Ohigashi, H.; Ishikawa, O.; Gotoh, K.; Yamada, T.; Nagata, S.; Tomita, Y.; Eguchi, H.; Doki, Y.; Yano, M. Perineural invasion and lymph node involvement as indicators of surgical outcome and pattern of recurrence in the setting of preoperative gemcitabine-based chemoradiation therapy for resectable pancreatic cancer. Ann. Surg. 2012, 255, 95–102. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marchegiani, G.; Andrianello, S.; Malleo, G.; De Gregorio, L.; Scarpa, A.; Mino-Kenudson, M.; Maggino, L.; Ferrone, C.R.; Lillemoe, K.D.; Bassi, C.; et al. Does Size Matter in Pancreatic Cancer? Reappraisal of Tumour Dimension as a Predictor of Outcome Beyond the TNM. Ann. Surg. 2017, 266, 142–148. [Google Scholar] [CrossRef]
- Hwang, H.K.; Jung, M.J.; Lee, S.H.; Kang, C.M.; Lee, W.J. Adverse oncologic effects of intraoperative transfusion during pancreatectomy for left-sided pancreatic cancer: The need for strict transfusion policy. J. Hepatobiliary Pancreat. Sci. 2016, 23, 497–507. [Google Scholar] [CrossRef] [PubMed]
- Blumberg, N. Deleterious clinical effects of transfusion immunomodulation: Proven beyond a reasonable doubt. Transfusion 2005, 45, 33–39. [Google Scholar] [CrossRef] [PubMed]
- Refaai, M.A.; Blumberg, N. Transfusion immunomodulation from a clinical perspective: An update. Expert. Rev. Hematol. 2013, 6, 653–663. [Google Scholar] [CrossRef] [PubMed]
- Kneuertz, P.J.; Patel, S.H.; Chu, C.K.; Maithel, S.K.; Sarmiento, J.M.; Delman, K.A.; Staley, C.A.; Kooby, D.A. Effects of perioperative red blood cell transfusion on disease recurrence and survival after pancreaticoduodenectomy for ductal adenocarcinoma. Ann. Surg. Oncol. 2011, 18, 1327–1334. [Google Scholar] [CrossRef]
- Clark, E.; Connor, S.; Taylor, M.A.; Hendry, C.L.; Madhavan, K.K.; Garden, O.J.; Parks, R.W. Perioperative transfusion for pancreaticoduodenectomy and its impact on prognosis in resected pancreatic ductal adenocarcinoma. HPB 2007, 9, 472–477. [Google Scholar] [CrossRef] [Green Version]
- Sutton, J.M.; Kooby, D.A.; Wilson, G.C.; Squires, M.H.; Hanseman, D.J.; Maithel, S.K.; Bentrem, D.J.; Weber, S.M.; Cho, C.S.; Winslow, E.R.; et al. Perioperative blood transfusion is associated with decreased survival in patients undergoing pancreaticoduodenectomy for pancreatic adenocarcinoma: A multi-institutional study. J. Gastrointest. Surg. 2014, 18, 1575–1587. [Google Scholar] [CrossRef] [PubMed]
- Paulson, A.S.; Tran Cao, H.S.; Tempero, M.A.; Lowy, A.M. Therapeutic advances in pancreatic cancer. Gastroenterology 2013, 144, 1316–1326. [Google Scholar] [CrossRef]
- Mohammed, S.; Van Buren, G.; Fisher, W.E. Pancreatic cancer: Advances in treatment. World J. Gastroenterol. 2014, 20, 9354–9360. [Google Scholar] [CrossRef] [PubMed]
- Sarris, E.G.; Syrigos, K.N.; Saif, M.W. Pancreatic cancer: Updates on translational research and future applications. JOP 2013, 14, 145–148. [Google Scholar] [CrossRef] [PubMed]
- Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics. CA Cancer J. Clin. 2020, 70, 7–30. [Google Scholar] [CrossRef] [PubMed]
- Kang, C.M.; Kim, D.H.; Choi, G.H.; Kim, K.S.; Choi, J.S.; Lee, W.J. Detrimental effect of postoperative complications on oncologic efficacy of R0 pancreatectomy in ductal adenocarcinoma of the pancreas. J. Gastrointest. Surg. 2009, 13, 907–914. [Google Scholar] [CrossRef]
- Kanda, M.; Kobayashi, D.; Tanaka, C.; Iwata, N.; Yamada, S.; Fujii, T.; Nakayama, G.; Sugimoto, H.; Koike, M.; Nomoto, S.; et al. Adverse prognostic impact of perioperative allogeneic transfusion on patients with stage II/III gastric cancer. Gastric Cancer 2016, 19, 255–263. [Google Scholar] [CrossRef] [Green Version]
- Luan, H.; Ye, F.; Wu, L.; Zhou, Y.; Jiang, J. Perioperative blood transfusion adversely affects prognosis after resection of lung cancer: A systematic review and a meta-analysis. BMC Surg. 2014, 14, 34. [Google Scholar] [CrossRef] [Green Version]
- Cata, J.P.; Wang, H.; Gottumukkala, V.; Reuben, J.; Sessler, D.I. Inflammatory response, immunosuppression, and cancer recurrence after perioperative blood transfusions. Br. J. Anaesth. 2013, 110, 690–701. [Google Scholar] [CrossRef] [Green Version]
- Liu, L.; Wang, Z.; Jiang, S.; Shao, B.; Liu, J.; Zhang, S.; Zhou, Y.; Zhou, Y.; Zhang, Y. Perioperative allogenenic blood transfusion is associated with worse clinical outcomes for hepatocellular carcinoma: A meta-analysis. PLoS ONE 2013, 8, e64261. [Google Scholar] [CrossRef] [Green Version]
- Komatsu, Y.; Orita, H.; Sakurada, M.; Maekawa, H.; Hoppo, T.; Sato, K. Intraoperative blood transfusion contributes to decreased long-term survival of patients with esophageal cancer. World J. Surg. 2012, 36, 844–850. [Google Scholar] [CrossRef] [PubMed]
- Zhang, R.C.; Zhang, B.; Mou, Y.P.; Xu, X.W.; Zhou, Y.C.; Huang, C.J.; Zhou, J.Y.; Jin, W.W.; Lu, C. Comparison of clinical outcomes and quality of life between laparoscopic and open central pancreatectomy with pancreaticojejunostomy. Surg. Endosc. 2017, 31, 4756–4763. [Google Scholar] [CrossRef] [PubMed]
- Yi, X.; Chen, S.; Wang, W.; Zou, L.; Diao, D.; Zheng, Y.; He, Y.; Li, H.; Luo, L.; Xiong, W.; et al. A Systematic Review and Meta-Analysis of Laparoscopic and Open Distal Pancreatectomy of Nonductal Adenocarcinomatous Pancreatic Tumor (NDACPT) in the Pancreatic Body and Tail. Surg. Laparosc. Endosc. Percutan. Tech. 2017, 27, 206–219. [Google Scholar] [CrossRef] [PubMed]
- Chen, K.; Pan, Y.; Zhang, B.; Maher, H.; Cai, X.J. Laparoscopic versus open pancreatectomy for pancreatic ductal adenocarcinoma: A systematic review and meta-analysis. Int. J. Surg. 2018, 53, 243–256. [Google Scholar] [CrossRef]
- Bauman, M.D.; Becerra, D.G.; Kilbane, E.M.; Zyromski, N.J.; Schmidt, C.M.; Pitt, H.A.; Nakeeb, A.; House, M.G.; Ceppa, E.P. Laparoscopic distal pancreatectomy for pancreatic cancer is safe and effective. Surg. Endosc. 2018, 32, 53–61. [Google Scholar] [CrossRef]
- Zhang, J.; Wu, W.M.; You, L.; Zhao, Y.P. Robotic versus open pancreatectomy: A systematic review and meta-analysis. Ann. Surg. Oncol. 2013, 20, 1774–1780. [Google Scholar] [CrossRef]
- Liu, R.; Liu, Q.; Zhao, Z.M.; Tan, X.L.; Gao, Y.X.; Zhao, G.D. Robotic versus laparoscopic distal pancreatectomy: A propensity score-matched study. J. Surg. Oncol. 2017, 116, 461–469. [Google Scholar] [CrossRef]
- Peng, L.; Zhou, Z.; Cao, Z.; Wu, W.; Xiao, W.; Cao, J. Long-Term Oncological Outcomes in Laparoscopic Versus Open Pancreaticoduodenectomy for Pancreatic Cancer: A Systematic Review and Meta-Analysis. J. Laparoendosc. Adv. Surg. Tech. A 2019, 29, 759–769. [Google Scholar] [CrossRef]
- Croome, K.P.; Farnell, M.B.; Que, F.G.; Reid-Lombardo, K.M.; Truty, M.J.; Nagorney, D.M.; Kendrick, M.L. Total laparoscopic pancreaticoduodenectomy for pancreatic ductal adenocarcinoma: Oncologic advantages over open approaches? Ann. Surg. 2014, 260, 633–638. [Google Scholar] [CrossRef]
Variables | Value |
---|---|
Age (years) | 62.5 ± 9.5 |
Sex | |
Female | 113 (39.4) |
Male | 174 (60.6) |
Past history | |
No | 75 (26.1) |
Yes | 212 (73.9) |
Symptoms | |
No | 57 (19.9) |
Yes | 230 (80.1) |
Complications (Clavien-Dindo Classification) | |
None | 135 (47.0) |
Grade 1 | 98 (34.1) |
Grade 2 | 17 (5.9) |
Grade 3 | 24 (8.4) |
Grade 4 | 10 (3.5) |
Grade 5 | 3 (1.0) |
T status | |
T0, T1, T2 | 262 (91.3) |
T3, T4 | 25 (8.7) |
N status | |
N0 | 137 (47.7) |
N1, N2 | 150 (52.3) |
Preoperative CA19_9 | 719.6 ± 202.7 |
Neo CRT (Neoadjuvant chemoradiation therapy) | |
No | 206 (71.8) |
Yes | 81 (28.2) |
Adj. CTx (Adjuvant chemotherapy) | |
No | 76 (26.5) |
Yes | 211 (73.5) |
Tumor location | |
Head | 111 (38.7) |
Uncinate | 66 (23.0) |
Neck | 6 (2.1) |
Body | 63 (22.0) |
Tail | 35 (12.2) |
Body + tail | 6 (2.1) |
LVI (Lymphovascular invasion) | |
No | 198 (69.0) |
Yes | 89 (31.0) |
PNI (Perineural invasion) | |
No | 106 (36.9) |
Yes | 181 (63.1) |
Resectability | |
Resectable | 215 (74.9) |
Borderline | 72 (25.1) |
Surgery type | |
PD | 17 (5.9) |
PPPD | 162 (56.4) |
DP | 101 (35.2) |
TP | 7 (2.4) |
Operation time (min) | 392.6 ± 148.5 |
Combined resection | |
No | 194 (67.6) |
Yes | 93 (32.4) |
Curative resection | |
R0 | 249 (86.8) |
R1 | 34 (11.8) |
R2 | 4 (1.4) |
EBL (mL) | 654.8 ± 215.5 |
IOT | |
No | 218 (76.0) |
Yes | 69 (24.0) |
Variables | Disease-Specific Survival (Event = 162) | Recurrence (Event = 191) | ||
---|---|---|---|---|
HR (95% CI) | P-Value | HR (95% CI) | P-Value | |
Age | 0.476 | 0.505 | ||
<63 | Ref | Ref | ||
≥63 | 1.12 (0.81–1.53) | 0.90 (0.68–1.20) | ||
Sex | 0.156 | 0.683 | ||
Male | Ref | Ref | ||
Female | 1.36 (0.99–1.88) | 1.06 (0.79–1.41) | ||
Past history | 0.716 | 0.741 | ||
No | Ref | Ref | ||
Yes | 1.06 (0.75–1.49) | 0.94 (0.69–1.30) | ||
Symptoms | 0.127 | 0.118 | ||
No | Ref | Ref | ||
Yes | 1.27 (0.93–1.74) | 1.24 (0.94–1.67) | ||
Complications | 0.28 | 0.734 | ||
None | Ref | Ref | ||
Grade 1 | 0.88 (0.63–1.25) | 0.94 (0.68–1.29) | ||
Grade 2 | 0.65 (0.30–1.41) | 0.64 (0.32–1.27) | ||
Grade 3 | 0.45 (0.22–0.89) | 0.64 (0.37–1.12) | ||
Grade 4 | 0.66 (0.27–1.64) | 1.32 (0.64–2.73) | ||
Grade 5 | 1.04 (0.25–4.29) | 0.49 (0.06–3.53) | ||
T status | 0.033 | 0.482 | ||
T0/T1/T2 | Ref | Ref | ||
T3/T4 | 1.75 (1.04–2.95) | 1.20 (0.71–2.00) | ||
N status | 0.002 | 0.668 | ||
N0 | Ref | Ref | ||
N1/N2 | 1.65 (1.20–2.26) | 1.05 (0.79–1.40) | ||
Preoperative CA19_9 | 0.796 | 0.553 | ||
<750 | Ref | Ref | ||
≥750 | 1.05 (0.72–1.53) | 1.10 (0.78–1.56) | ||
NeoCRT | 0.711 | 0.612 | ||
No | Ref | Ref | ||
Yes | 0.96 (0.68–1.36) | 1.08 (0.79–1.48) | ||
Adj CTx | 0.061 | 0.082 | ||
No | Ref | Ref | ||
Yes | 0.68 (0.49–0.96) | 0.86 (0.62–1.19) | ||
Tumor location | 0.375 | 0.824 | ||
Head | Ref | Ref | ||
Uncinate | 1.09 (0.71–1.68) | 1.04 (0.71–1.51) | ||
Neck | 2.66 (1.06–6.68) | 2.80 (1.12–7.01) | ||
Body | 0.88 (0.58–1.34) | 0.71 (0.47–1.05) | ||
Tail | 1.61 (1.01–2.57) | 1.53 (0.99–2.37) | ||
Body + Tail | 0.59 (0.18–1.88) | 0.45 (0.14–1.44) | ||
LVI | 0.084 | 0.292 | ||
No | Ref | Ref | ||
Yes | 1.33 (0.96–1.84) | 1.17 (0.86–1.59) | ||
PNI | 0.597 | 0.393 | ||
No | Ref | Ref | ||
Yes | 1.08 (0.79–1.49) | 1.13 (0.84–1.52) | ||
Resectability | 0.459 | 0.23 | ||
Resectable | Ref | Ref | ||
Borderline | 0.86 (0.59–1.25) | 1.21 (0.88–1.67) | ||
Surgery type | 0.08 | 0.202 | ||
PD | Ref | Ref | ||
PPPD | 0.58 (0.31–1.06) | 1.55 (0.78–3.06) | ||
DP | 0.56 (0.30–1.04) | 1.23 (0.61–2.50) | ||
TP | 1.23 (0.34–4.39) | 4.66 (1.72–12.58) | ||
Operation time | 0.778 | 0.845 | ||
<400 | Ref | Ref | ||
≥400 | 1.05 (0.73–1.51) | 1.03 (0.73–1.45) | ||
Combined resection | 0.285 | 0.07 | ||
No | Ref | Ref | ||
Yes | 1.19 (0.86–1.66) | 1.31 (0.97–1.77) | ||
Curative resection | 0.703 | 0.765 | ||
R0 | Ref | Ref | ||
R1/R2 | 1.09 (0.68–1.75) | 0.93 (0.59–1.45) | ||
EBL | 0.778 | 0.646 | ||
<650 | Ref | Ref | ||
≥650 | 1.03 (0.73–1.51) | 1.06 (0.80–1.42) | ||
IOT | 0.011 | 0.031 | ||
No | Ref | Ref | ||
Yes | 1.55 (1.10–2.17) | 1.41 (1.03–1.94) | ||
Period | 0.631 | 0.772 | ||
2004–2007 | Ref | Ref | ||
2008–2011 | 1.04 (0.71–1.52) | 1.05 (0.72–1.54) | ||
2012–2014 | 0.89 (0.57–1.40) | 1.67 (0.72–1.59) |
Variables | Disease-Specific Survival (Event = 162) | Recurrence (Event = 191) | ||
---|---|---|---|---|
HR (95% CI) | P-Value | HR (95% CI) | P-Value | |
T status | 0.018 | |||
T0/T1/T2 | Ref | |||
T3/T4 | 2.04 (1.13–3.68) | |||
N status | 0.045 | |||
N0 | Ref | |||
N1, N2 | 1.46 (1.00–2.12) | |||
LVI | 0.225 | |||
No | Ref | |||
Yes | 1.25 (0.86–1.82) | |||
Surgery type | 0.126 | |||
PD | Ref | |||
PPPD | 0.43 (0.20–0.89) | |||
DP | 0.41 (0.13–1.28) | |||
TP | 0.97 (0.22–4.25) | |||
Adj.CTx | 0.001 | 0.035 | ||
No | Ref | Ref | ||
Yes | 0.51 (0.35–0.75) | 0.67 (0.46–0.97) | ||
IOT | 0.004 | 0.056 | ||
No | Ref | Ref | ||
Yes | 1.94 (1.23–3.07) | 1.47 (0.99–2.20) | ||
Combined resection | 0.727 | |||
No | Ref | |||
Yes | 0.93 (0.64–1.35) |
Variables | IOT | P-Value | |
---|---|---|---|
No (n = 218) | Yes (n = 69) | ||
Age | 0.356 | ||
<63 | 96 (44.0) | 26 (37.7) | |
≥63 | 122 (56.0) | 43 (62.3) | |
Sex | 0.747 | ||
Male | 87 (39.9) | 26 (37.7) | |
Female | 131 (60.1) | 43 (62.3) | |
Past history | 0.751 | ||
No | 58 (26.6) | 17 (24.6) | |
Yes | 160 (73.4) | 52 (75.4) | |
Symptoms | 0.189 | ||
No | 53 (24.3) | 4 (5.7) | |
Yes | 165 (75.6) | 65 (94.3) | |
Complications | 0.293 | ||
None | 101 (46.3) | 34 (49.3) | |
Grade 1 | 76 (34.9) | 22 (31.9) | |
Grade 2 | 11 (5.0) | 6 (8.7) | |
Grade 3 | 22 (10.1) | 2 (2.9) | |
Grade 4 | 6 (2.8) | 4 (5.8) | |
Grade 5 | 2 (0.9) | 1 (1.4) | |
T status | 0.638 | ||
T0/T1/T2 | 200 (91.7) | 62 (89.9) | |
T3/T4 | 18 (8.3) | 7 (10.1) | |
N status | 0.285 | ||
N0 | 108 (49.5) | 29 (42.0) | |
N1/N2 | 110 (50.5) | 40 (58.0) | |
Preoperative CA19_9 | 0.058 | ||
<750 | 178 (81.7) | 49 (71.0) | |
≥750 | 40 (18.3) | 20 (29.0) | |
NeoCRT | 0.167 | ||
No | 168 (77.1) | 38 (55.1) | |
Yes | 50 (22.9) | 31 (44.9) | |
Adj CTx | 0.932 | ||
No | 58 (26.6) | 18 (26.1) | |
Yes | 160 (73.4) | 51 (73.9) | |
Tumor location | 0.065 | ||
Head | 74 (33.9) | 37 (53.6) | |
Uncinate | 50 (22.9) | 20 (23.2) | |
Neck | 6 (2.8) | 0 (0.0) | |
Body | 50 (22.9) | 13 (18.8) | |
Tail | 32 (14.7) | 3 (4.3) | |
Body + Tail | 6 (2.8) | 0 (0.00) | |
LVI | 0.276 | ||
No | 146 (67.0) | 52 (75.4) | |
Yes | 72 (33.0) | 17 (24.6) | |
PNI | 0.674 | ||
No | 78 (35.8) | 28 (40.6) | |
Yes | 140 (64.2) | 41 (59.4) | |
Resectability | 0.651 | ||
Resectable | 175 (80.3) | 40 (58.0) | |
Borderline | 43 (19.7) | 29 (42.0) | |
Surgery type | |||
PD | 13 (6.0) | 4 (5.8) | |
PPPD | 114 (52.3) | 48 (69.6) | |
DP | 87 (39.9) | 14 (20.3) | |
TP | 4 (1.8) | 3 (4.3) | |
Operation time | 0.064 | ||
<400 | 123 (56.4) | 14 (20.3) | |
≥400 | 95 (43.6) | 55 (79.7) | |
Combined resection | <.0.001 | ||
No | 167 (76.6) | 27 (39.1) | |
Yes | 51 (23.4) | 42 (60.9) | |
Curative resection | 0.641 | ||
R0 | 188 (86.2) | 61 (88.4) | |
R1/R2 | 30 (13.8) | 8 (11.6) | |
EBL | <0.001 | ||
<650 | 145 (66.5) | 10 (14.5) | |
≥650 | 73 (33.5) | 59 (85.5) | |
Period | 0.004 | ||
2004–2007 | 40 (18.3) | 16 (23.2) | |
2008–2011 | 79 (36.2) | 37 (53.6) | |
2012–2014 | 99 (45.4) | 16 (23.2) |
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Kim, S.Y.; Choi, M.; Hwang, H.K.; Rho, S.Y.; Lee, W.J.; Kang, C.M. Intraoperative Transfusion is Independently Associated with a Worse Prognosis in Resected Pancreatic Cancer—a Retrospective Cohort Analysis. J. Clin. Med. 2020, 9, 689. https://doi.org/10.3390/jcm9030689
Kim SY, Choi M, Hwang HK, Rho SY, Lee WJ, Kang CM. Intraoperative Transfusion is Independently Associated with a Worse Prognosis in Resected Pancreatic Cancer—a Retrospective Cohort Analysis. Journal of Clinical Medicine. 2020; 9(3):689. https://doi.org/10.3390/jcm9030689
Chicago/Turabian StyleKim, Si Youn, Munseok Choi, Ho Kyoung Hwang, Seoung Yoon Rho, Woo Jung Lee, and Chang Moo Kang. 2020. "Intraoperative Transfusion is Independently Associated with a Worse Prognosis in Resected Pancreatic Cancer—a Retrospective Cohort Analysis" Journal of Clinical Medicine 9, no. 3: 689. https://doi.org/10.3390/jcm9030689