Clinical Impact of Unexpected Para-Aortic Lymph Node Metastasis in Surgery for Resectable Pancreatic Cancer

doi:10.21203/rs.3.rs-386384/v1

Download PDF

Research Article

Clinical Impact of Unexpected Para-Aortic Lymph Node Metastasis in Surgery for Resectable Pancreatic Cancer

https://doi.org/10.21203/rs.3.rs-386384/v1

This work is licensed under a CC BY 4.0 License

Journal Publication

published 03 Sep, 2021

Read the published version in Cancers →

Version 1

posted

You are reading this latest preprint version

Radiologically identified para-aortic lymph node (PALN) metastasis is contraindicated for pancreatic cancer (PC) surgery. There is no clinical consensus for unexpected intraoperative PALN. To analyse the prognostic role of unexpected PALN in resectable PC, we retrospectively reviewed data of 1,953 PC patients in a single tertiary centre. Patients with intraoperative PALN without radiological PALN (group A1, negative pathology, n = 59; group A2, positive pathology, n = 13) showed median overall survival (OS) of 24.6 (95% confidence interval [CI]: 15.2–33.2) and 13.0 (95%CI: 4.9–19.7) months, respectively. Patients with radiological PALN metastasis without other metastases (group B, n = 91) showed median OS of 8.6 months (95%CI: 7.4–11.6). Compared with group B, groups A1 and A2 had hazard ratios (HRs) of 0.37 (95%CI, 0.2–0.6) and 1.04 (95%CI: 0.7–1.4), respectively. Compared with group A2, group A1 had HR of 0.33 (95%CI: 0.2–0.7). Analysing regional lymph nodes (LNs), the positive LN ratio affected survival (HR: 2.67, 95%CI: 1.6–4.5), while the absolute number of positive LNs (HR: 1.79, 95%CI: 0.7–4.6) did not. Thus, unexpected malignant PALN has a negative prognostic impact comparable to radiological PALN metastasis. Prompt pathologic evaluation for unexpected PALN and maximal harvest of regional LNs during PC surgery are suggested.

Cancer Biology

Oncology

Gastrointestinal Surgery

PALN

pancreatic cancer

overall survival

Para-aortic

Pancreatic ductal adenocarcinoma is the second most common gastrointestinal cancer in the United States and is responsible for 43,000 deaths annually¹. It is one of the most aggressive tumours, with a 1-year mortality rate of 20–25%^2–4. Approximately 80% of patients with pancreatic cancer (PC) are diagnosed with metastatic lesions. Surgical resection is the only curative treatment for patients with no distant metastasis.

Previous studies on PC have shown that regional lymph node (LN) metastasis results in poor prognosis^5–7. The American Joint Committee on Cancer (AJCC) 8th edition defines N stage according to the number of regional LN metastases⁸. In addition to regional LNs, the definition of metastatic LNs depends on the location of the primary tumour, either in the head or tail⁸.

In both pancreatic head and pancreatic tail cancers, para-aortic LN (PALN) metastasis is defined as distant metastasis⁸. PALN metastasis may imply systemic illness with aggressive tumour behaviour, resulting in a grave prognosis. Previous studies showed that radiologically observed PALN metastasis correlates directly with poor prognosis^9–11. Therefore, patients with radiologically observed PALN metastasis preoperatively are recommended to undergo chemotherapy or radiotherapy rather than surgical resection.

Nevertheless, when surgeons discover unexpected PALN enlargement during surgery, which was not recognised in preoperative imaging studies, there is no definite consensus on whether there should be any change in the treatment strategy. In this study, we evaluated the prognostic value of unexpected PALN metastasis in patients with clinically resectable PC with no other distant metastases.

Baseline characteristics

A total of 1,953 patients were diagnosed with pancreatic ductal adenocarcinoma from January 2004 to December 2019 (Fig. 1). Patients were categorised according to their clinical stages. In the clinical staging based on the imaging studies, a total of 440 patients were diagnosed with resectable PC, 455 were diagnosed with locally advanced PC, and 1,059 were diagnosed with metastatic PC.

Among 440 resectable PC patients, a total of 358 patients underwent curative resection for pancreatic cancer. Among them, unexpected intraoperative PALN enlargement was found in 72 patients, who were categorised as group A. Based on the final pathologic report, patients with benign PALN were categorised into group A1 (n = 59), and those with malignant PALN were categorised into group A2 (n = 13).

Among 1,059 patients with metastatic PC, ninety-one patients had no distant metastasis other than PALN metastasis and were categorised as group B.

No significant difference was observed in the baseline demographic information among the three patient groups (Table 1).

Table 1

Patient’s baseline characteristics
Variable	Group A1 (n = 59)	Group A2 (n = 13)	Group B (n = 91)	Total patients (n = 163)
Age (years)	63 (53–72)	60 (57–66)	67 (60–76)	65 (58–74)
Sex
Male	29 (49.1)	5 (38.5)	45 (49.5)	79 (48.5)
Female	30 (50.8)	8 (61.5)	46 (50.6)	84 (51.5)
BMI	22.1 (20.5–23.9)	21.30 (19.7–23.5)	22.58 (20.7–25.0)	22.33 (20.5–24.8)
Initial tumour markers
CA 19 − 9	101.8 (38.2–430)	191.9 (41–1653.75)	240 (74–731.3)	180.9 (49–607.5)
CEA	2.9 (1.4–5.15)	4.9 (3.6–5.4)	2.55 (1.9– 5)	2.8 (1.65–5.1)
Tumour location
Head	49 (83.1)	13 (100)	62 (68.1)	124 (76.1)
Body	7 (11.9)	0	15 (16.5)	22 (13.5)
Tail	2 (3.3)	0	11 (12.1)	13 (8.0)
Multiple	1 (1.7)	0	3 (3.3)	4 (2.4)
Tumour size (cm)
	2.7 (2–3.3)	2.7 (2.1–3.3)	3.2 (2.5–4.2)	3.00 (2.4–3.9)
Concomitant Regional lymph node	5 (8.5)	1 (7.7)	39 (42.9)	45 (27.6)
Data are presented as median (interquartile range) or number of patients (%), unless otherwise stated.

Survival of patients with unexpected PALN

Figure 2 and Table 2 shows the overall survival of the three patient groups. The median survival of patients in group B was 8.6 months, and that of patients in group A1 was 24.6months, (hazard ratio [HR]: 0.37, 95% confidence interval [CI]: 0.2–0.7, P < 0.001) compared to group B). On contrary, the median survival of patients in group A2 was 13.0 months (HR: 1.04, 95% CI: 0.7–1.4, P = 0.905, compared to group B).

Table 2

Univariate and multivariate analyses
Variable (n)	Median Survival(month)	95% CI	Univariate			Multivariate
Variable (n)	Median Survival(month)	95% CI	HR	95% CI	P-value	HR	95% CI	P-value
Overall patients	14.6	11.1–17.1
Sex
Male (67)	16.9	11.5–20.4	–
Female (67)	13.0	8.8–15.5	0.92	0.6–1.3	0.680
Age
Age ≤ 65 (65)	19.6	14.9–27.4	–			–
Age > 65 (69)	8.7	6.6–13.0	1.98	1.4–2.9	0.000	1.73	1.1–2.7	0.012
BMI
BMI ≤ 22.33 (61)	14.8	10.3–17.1	–
BMI > 22.33 (54)	21.5	11.1–29.3	0.70	0.5–1.1	0.089
Group (ref B)
Group B	8.6	7.4–11.6	–
Group A2	13.0	4.9–19.7	1.04	0.7–1.4	0.905	1.49	0.7–3.1	0.289
Group A1	24.6	15.2–33.2	0.37	0.2–0.6	0.000	0.58	0.3–0.9	0.041
Group (ref A2) *						–
Group A2	13.0	4.9–19.7	–			–
Group A1	24.6	15.2–33.2	0.33	0.2–0.7	0.003	–
Regional lymph node
No metastasis	14.9	11.2–20.4
Metastasis	11.6	7.9–16.5	1.69	1.1–2.5	0.010	1.32	0.8–2.3	0.315
CA19–9
CA19–9 ≤ 180 (60)	21.5	14.5–28.8	–			–
CA19–9 > 180 (56)	11.6	9.2–15.5	1.70	1.1–2.6	0.011	1.49	0.97–2.3	0.067
CEA
CEA ≤ 2.8 (39)	15.5	11.2–21.5	–
CEA > 2.8 (51)	13.0	8.0–18.3	1.16	0.7–1.8	0.543
Tumour size
Tumour size ≤ 3.0 (59)	14.8	11.2–24.6
Tumour size > 3.0 (75)	13.0	8.5–18.0	1.43	1.0–2.1	0.069
*Not applied in the multivariate analysis

Other prognostic factors affecting overall survival

Table 2 shows other factors affecting the overall survival. Sex, body mass index (BMI) at diagnosis, initial carcinoembryonic antigen (CEA), and tumour size failed to show a significant difference in patient survival. No significant survival difference was observed between patients in group B and those in group A2 (HR: 1.04, 95% CI: 0.7–1.4, P = 0.905). Patients in group A1 had significantly better prognosis than those in group B (HR: 0.37, 95% CI: 0.2–0.6, P < 0.000).

Multivariate analysis showed no prognostic significance according to the initial CA19-9 level or regional LN status. Multivariate analysis still showed significantly better survival in group A1 than in group B (HR: 0.58, 95% CI: 0.3–0.9, P = 0.041).

Surgical information including postoperative complications

Surgical information of groups A1 and A2 is summarised in Table 3. No significant differences were found in the operation type, the most common being pancreaticoduodenectomy. The total numbers of LNs resected were 24 in group A1 and 25 in group A2. The numbers of para-aortic LNs resected were 17 in group A1 and 22 in group A2. The positive LN ratio (LNR) is defined as the ratio of the number of positive LNs to the total number of LNs harvested during surgery. The median LNR in group A1 was 5.6 and that in group A2 was 26 months (P = 0.0002).

Table 3

Surgical information of groups A1 and A2
Patient Group (n, %)	A1 (59, 100%)	A2 (13, 100%)	P-value
OP type			0.477
Pancreaticoduodenectomy^*	47 (80%)	11 (85%)
Distal pancreatectomy	5 (8.5%)	0 (0%)
Total pancreatectomy	5 (8.5%)	1 (7.5%)
Others^†	2 (3.4%)	1 (7.5%)
Resection margin			0.272
Negative	41 (69%)	6 (46%)
Positive	14 (24%)	5 (38%)
Overall number of dissected LN (median, IQR)	24 (16–33)	25 (15–32)	0.915
No of dissected PALN	5 (2–9)	3 (1–5)	0.117
No of dissected regional LN	17 (11–25)	22 (12–31)	0.476
Pathologic T staging			0.505
Tx	0 (0%)	2 (15%)
T1–T2	47 (80%)	10 (77%)
T3–T4	12 (20%)	1 (8%)
Pathologic N staging			0.191
Nx	2 (3%)	2 (15%)
N0	27 (46%)	0 (0%)
N1	33 (56%)	3 (23%)
N2	7 (12%)	8 (62%)
Ratio of positive LN (%)^‡
	8.1 (0–30.7)	26.67 (0–51.9)	0.0002
Pathologic M staging ^§
M0	58 (98%)	0 (0%)
M1	1 (2%)	11 (100%)
Moderate to severe surgical complication
All complication	32 (54%)	4 (31%)	0.163
Surgical site infection	4 (7%)	1 (8%)	0.826
Postoperative haemorrhage	4 (7%)	0 (0%)	0.831
Pancreas fistula	9 (15%)	0 (0%)	0.344
Liver abscess	1 (2%)	0 (0%)	0.647
Others^∥	14 (24%)	3 (23%)
Data are presented number of patients (%), unless otherwise stated.
*Pancreaticoduodenectomy includes PPPD, PRPD, and Whipple operation.
†Others included palliative cholecystectomy and O&C.
‡ includes PALN
§Because groups A1 and A2 had no metastasis other than distant LN metastasis, M stage depends only on the presence or absence of distant LN metastasis
∥Others include chylous ascites, bacteraemia, acute kidney injury, postoperative ileus, and cholangitis.

The number of surgical complications did not differ between the two patient groups. (Table 3) The most common surgical complications in the two patient groups were pancreatic fistula, followed by surgical site infection and postoperative haemorrhage.

Effects of overall lymph node status

Patient survival was analysed based on the number of metastatic LNs (LNS) (Fig. 3A). Patients were grouped as follows: those with fewer than four metastatic LNs and those with more than three metastatic LNs. The median survival of patients with less than four metastatic LNs was 22.5 months and that of patients with more than three metastatic LNs was 4.4 months (HR: 1.79, 95% CI: 0.7–4.6, P = 0.233).

Patient survival was also analysed based on the LNR (Fig. 3B). The median LNR was 4.2%. We categorised the patients into two groups: patients with LNR ≤ 4.2% and patients with LNR > 4.2%. The median survival of patients with lower LNR was 38.6 months and that of patients with higher LNR was 15.2 months (HR: 2.67, 95% CI: 1.6–4.5, P < 0.001).

Other medical information

Non-surgical therapies performed in patients are summarised in Table 4. The most common first-line palliative chemotherapy regimen was FOLFIRINOX. Gemcitabine monotherapy was the most common adjuvant therapy regimen.

Table 4

Treatment information other than surgery
Patient Group (n, %)	A1 (59)	A2 (13)	B (91)	P-value
First-line palliative chemotherapy*				0.036
FOLFIRINOX	2 (3.4%)	3 (23.1%)	18 (19.8%)
Gemcitabine with nab-paclitaxel	0 (0%)	0 (0%)	5 (5.5%)
Gemcitabine monotherapy	1 (1.7%)	1 (7.7%)	6 (6.6%)
Other gemcitabine-based chemotherapy	3 (5.1%)	1 (7.7%)	12 (13.2%)
Adjuvant chemotherapy				0.164
FOLFIRINOX	1 (1.7%)	0 (0%)	3 (3.3%)
Other 5-FU-based regimen	1 (1.7%)	0 (0%)	0 (0%)
Gemcitabine monotherapy	28 (47.5%)	3 (23.1%)	6 (6.6%)
Other gemcitabine-based chemotherapy	5 (8.5%)	1 (7.7%)	3 (3.3%)
Radiation therapy				0.038
Yes	37 (62.7%)	9 (69.2%)	73 (80.2%)
No	22 (37.3%)	4 (30.8%)	18 (19.8%)
Data are presented as number of patients (%).
*Palliative chemotherapy after tumour recurrence is excluded.

The ratio of patients receiving radiotherapy varied among the three patient groups. Seventy-three out of 91 patients in group B (80%) received radiotherapy, 9 out of 13 patients in group A2 (69.2%), while 37 out of 59 patients in group A1 (62.7%) received radiotherapy.

This study was a retrospective analysis of the prognostic role of unexpected PALN metastasis in PC. In our study, unexpected intraoperative PALN metastasis resulted in shorter patient survival. Additionally, this study showed that the number of metastatic LNs was not a determinant of prognosis. On the contrary, patients with high LNR showed worse prognosis than those with low LNR.

In PC, the prognostic role of distant metastasis has been well established in various studies^14–16. Nevertheless, the prognostic value of PALN metastasis has not been firmly established.^{9–11, 17, 18} When unexpected PALN enlargement is found during curative resection of PC, there is no consensus on whether additional treatment strategies will be implemented. A systematic review and meta-analysis by Paiella suggested that PALN metastasis correlates with poor prognosis in patients with pancreatic adenocarcinoma.⁹ On the contrary, a multicentre study by Masayuki Sho suggested that some patients with PC having metastatic PALN may survive longer than expected after undergoing pancreatectomy.^{10, 17} Moreover, the prognosis of patients with ‘PALN metastasis only’ without other metastases remains unclear.

In this study, the patients were primarily categorised into two groups: group A, patients with radiologically resectable PC who had unexpected intraoperative PALN enlargement; and group B, patients with clinical metastatic PC having only PALN metastasis, with no evidence of other distant metastases. Patients in group A were further grouped into group A1, comprising patients with pathologically benign PALN, and group A2, comprising patients with pathologically proven PALN metastasis.

The median survival of patients in group B (median: 8.6 months, 95% CI: 15.2–33.2 months) was similar to historical data of that of metastatic PCs^{15,16, 19, 20}. Group A1 also showed similar overall survival of historical data of resectable PC^19,20. Therefore, median survival of patients in group A1 were significantly longer than that of patients in group B (HR: 0.37, 95% CI: 0.2–0.6, P < 0.001). The survival of patients in group A2 were not different from those of patients in group B (HR: 1.04, 95% CI: 0.7–1.4, P = 0.905).

Patients in group A1 had significantly longer median survival compared to that of group A2 (HR: 0.33, 95% CI: 0.2–0.7, P = 0.003). This result suggests negative prognostic impact of PALN, and surgeons are recommended to perform frozen biopsy for unexpected intraoperative PALN enlargements. This result is consistent with that of a systemic review by Paiella⁹.

In addition to PALN metastasis, the number of other LN metastases is an important confounding factor in this study. Various studies have reported that lymph node ratio, rather than absolute number of metastatic LN is inversely associated to survival^21–23. No significant survival differences were found according to the number of metastatic LNs. Nevertheless, patients with lower LNR had better prognosis than those with higher LNR. This result suggests that it is important for surgeons to harvest a sufficient number of LNs during surgery.

This study has a few limitations. The number of patients was relatively small. Nevertheless, the statistical analysis resulted in significant survival differences, and further studies with larger numbers of patients are warranted to yield more significant differences. Not all patients in the study had information on frozen biopsy, and we analysed the PALN metastasis status based on the final pathologic report. Nevertheless, Alexandre Doussot reported that frozen sections of PALN yielded accurate PALN assessment^{13, 24–26}.

In conclusion, unexpected malignant PALN could have a negative prognostic impact on the survival of patients with radiologically resectable PC comparing to those with clinically metastatic PALN. Patients with higher LNR had shorter survival than those with lower LNR. This study suggested that frozen sections need to be performed when unexpected PALN enlargement is found during surgery. Moreover, as LNR functions as an independent prognostic factor, surgeons are advised to harvest as many LNs as possible during curative surgery.

Patients

Medical and pathologic records of patients diagnosed with pancreatic adenocarcinoma in a single tertiary centre (Seoul National University Bundang Hospital) from 2004 to 2019 were retrospectively reviewed. Patients who were previously diagnosed with PC and treated with chemotherapy, radiotherapy, or surgery from other hospitals were excluded from the study. Patients with malignant tumours other than PC were also excluded.

Results of all imaging tests were reviewed and the patients categorised in accordance with the AJCC 8th edition⁸. Patients diagnosed with locally advanced PC and borderline resectable PC were excluded. Patients with metastatic PC were divided into those with PALN metastasis alone and those with other distant metastases.

Surgical records and pathology reports of patients with radiologically resectable PC, with clinical stage TxN0M0, were reviewed. Among patients who underwent surgical resection, those who had unexpected intraoperative PALN enlargement during surgery were categorised as group B. All patients in group B had para-aortic LN dissection, and the final pathologic diagnosis was made. Patients with negative para-aortic LNs were categorised as group A1, while those with positive para-aortic LNs were categorised as group A2 (Fig. 1). Patients with no other distant metastasis, but only PALN metastasis, were classified as patient group B.

Study design

This study was conducted as a single-centre, retrospective cohort study. The primary endpoint was the overall survival of patients.

Statistical analysis

Statistical analyses were performed using Stata version 15.0. Categorical data on the three patient groups were analysed using a 2 × 3 chi-square test or 2 × 3 Fisher’s exact test. Numerical data with a normal distribution were analysed using analysis of variance, and those that failed to follow a normal distribution were analysed using the Kruskal-Wallis test. Survival data were analysed using the Cox proportional hazard model. Categorical variables are expressed as percentages, and continuous variables are expressed as IQR. A p-value < 0.05 was considered to indicate statistical significance.

This study was approved by the institutional review board of Seoul National University Bundang Hospital (Protocol No. B-2104-681-105), and informed consent was waived. All procedures performed in this study were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Acknowledgements

We thank to Young Hoon Lee, Kyoung Ho Lee, Ji Hoon Park, Yoon Jin Lee, Chang Won, Hae Young Kim, the specialists in department of Radiology in Seoul National University Bundang Hospital. We would like to thank Editage (www.editage.co.kr) for English language editing.

Author contributions

Study concept and design by Lee HK, Yoon YS, Lee JC; Statistical analysis plan by Lee HK, Hwang JH, Lee JC; Data recruitment by Park JW, Jung KR; Data management by Lee HK, Jung JH, Kin JH, Lee JC; Pathologic data manipulation by Na HY, Ahn SM; Statistical analysis by Lee HK, Hwang JH, Lee JC; Visualization by Lee HK, Lee JC; Interpretation of result by Lee HK, Yoon YS, Lee JS, Han HS, Lee JC; Draft writing by Lee HK, Lee JS, Na HY, Lee JC; Draft revising by Lee HK, Han HS, Lee JS, Ahn SM, Park JW, Jung KR, Jung JH, Kim JH, Hwang JH, Lee JC

Competing interest

The authors declare no potential conflicts of interest, including patents, familial relationships, and affiliations with any organisation with direct or indirect financial interest in the subject matter discussed in the manuscript.

Siegel, R. L., Miller, K. D. & Jemal, A. Cancer Statistics, 2017. CA Cancer J Clin 67, 7–30, doi:10.3322/caac.21387 (2017).
Lim, J. E., Chien, M. W. & Earle, C. C. Prognostic factors following curative resection for pancreatic adenocarcinoma: a population-based, linked database analysis of 396 patients. Ann Surg. 237, 74–85 https://doi.org/10.1097/00000658-200301000-00011 (2003).
Chun, Y. S., Pawlik, T. M. & Vauthey, J. N. 8th Edition of the AJCC Cancer Staging Manual: Pancreas and Hepatobiliary Cancers. Ann Surg Oncol. 25, 845–847 https://doi.org/10.1245/s10434-017-6025-x (2018).
Paiella, S. et al. The prognostic impact of para-aortic lymph node metastasis in pancreatic cancer: A systematic review and meta-analysis. Eur J Surg Oncol. 42, 616–624 https://doi.org/10.1016/j.ejso.2016.02.003 (2016).
Agalianos, C., Gouvas, N., Papaparaskeva, K. & Dervenis, C. Positive para-aortic lymph nodes following pancreatectomy for pancreatic cancer. Systematic review and meta-analysis of impact on short term survival and association with clinicopathologic features. HPB (Oxford). 18, 633–641 https://doi.org/10.1016/j.hpb.2016.04.007 (2016).
Komo, T. et al. Prognostic Impact of Para-Aortic Lymph Node Micrometastasis in Pancreatic Ductal Adenocarcinoma. Ann Surg Oncol. 23, 2019–2027 https://doi.org/10.1245/s10434-016-5120-8 (2016).
Sho, M. et al. Postoperative prognosis of pancreatic cancer with para-aortic lymph node metastasis: a multicenter study on 822 patients. J Gastroenterol. 50, 694–702 https://doi.org/10.1007/s00535-014-1005-4 (2015).
Doussot, A. et al. Pancreatic ductal adenocarcinoma and paraaortic lymph nodes metastases: The accuracy of intraoperative frozen section. Pancreatology. 19, 710–715 https://doi.org/10.1016/j.pan.2019.05.465 (2019).
Wagner, M. et al. Curative resection is the single most important factor determining outcome in patients with pancreatic adenocarcinoma. Br J Surg. 91, 586–594 https://doi.org/10.1002/bjs.4484 (2004).
Richter, A. et al. Long-term results of partial pancreaticoduodenectomy for ductal adenocarcinoma of the pancreatic head: 25-year experience. World J Surg. 27, 324–329 https://doi.org/10.1007/s00268-002-6659-z (2003).
Coupland, V. H. et al. Incidence and survival for hepatic, pancreatic and biliary cancers in England between 1998 and 2007. Cancer Epidemiol. 36, e207–214 https://doi.org/10.1016/j.canep.2012.03.010 (2012).
Kim, J. S., Hwang, H. K., Lee, W. J. & Kang, C. M. Unexpected Para-aortic Lymph Node Metastasis in Pancrea Prognostic value of lymph node metastases detected during surgical exploration for pancreatic or periampullary cancer: a systematic review and meta-analysistic Ductal Adenocarcinoma: a Contraindication to Resection? J Gastrointest Surg. 24, 2789–2799 https://doi.org/10.1007/s11605-019-04483-8 (2020).
Sperti, C. et al. Para-aortic node involvement is not an independent predictor of survival after resection for pancreatic cancer. World J Gastroenterol. 23, 4399–4406 https://doi.org/10.3748/wjg.v23.i24.4399 (2017).
Kleeff, J. et al. Pancreatic cancer. Nat Rev Dis Primers. 2, 16022 https://doi.org/10.1038/nrdp.2016.22 (2016).
Gemenetzis, G. et al. Survival in Locally Advanced Pancreatic Cancer After Neoadjuvant Therapy and Surgical Resection. Ann Surg. 270, 340–347 https://doi.org/10.1097/sla.0000000000002753 (2019).
Fischer, L. K. et al. The number and ratio of positive lymph nodes affect pancreatic cancer patient survival after neoadjuvant therapy and pancreaticoduodenectomy. Histopathology. 68, 210–220 https://doi.org/10.1111/his.12732 (2016).
Mirkin, K. A., Hollenbeak, C. S. & Wong, J. Greater lymph node retrieval and lymph node ratio impacts survival in resected pancreatic cancer. J Surg Res. 220, 12–24 https://doi.org/10.1016/j.jss.2017.06.076 (2017).
Ashfaq, A., Pockaj, B. A., Gray, R. J., Halfdanarson, T. R. & Wasif, N. Nodal counts and lymph node ratio impact survival after distal pancreatectomy for pancreatic adenocarcinoma. J Gastrointest Surg. 18, 1929–1935 https://doi.org/10.1007/s11605-014-2566-5 (2014).
Schwarz, L. et al. Para-aortic lymph node sampling in pancreatic head adenocarcinoma. Br J Surg. 101, 530–538 https://doi.org/10.1002/bjs.9444 (2014).
Imai, H. et al. Preoperative assessment of para-aortic lymph node metastasis in patients with pancreatic cancer. Int J Clin Oncol. 15, 294–300 https://doi.org/10.1007/s10147-010-0066-5 (2010).
Karabagli, P., Ugras, S., Yilmaz, B. S. & Celik, C. The evaluation of reliability and contribution of frozen section pathology to staging endometrioid adenocarcinomas. Arch Gynecol Obstet. 292, 391–397 https://doi.org/10.1007/s00404-015-3621-5 (2015).
Mirkin, K. A., Hollenbeak, C. S. & Wong, J. Greater lymph node retrieval and lymph node ratio impacts survival in resected pancreatic cancer. J Surg Res 220, 12–24, doi:10.1016/j.jss.2017.06.076 (2017).
Ashfaq, A., Pockaj, B. A., Gray, R. J., Halfdanarson, T. R. & Wasif, N. Nodal counts and lymph node ratio impact survival after distal pancreatectomy for pancreatic adenocarcinoma. J Gastrointest Surg 18, 1929–1935, doi:10.1007/s11605-014-2566-5 (2014).
Schwarz, L. et al. Para-aortic lymph node sampling in pancreatic head adenocarcinoma. Br J Surg 101, 530–538, doi:10.1002/bjs.9444 (2014).
Imai, H. et al. Preoperative assessment of para-aortic lymph node metastasis in patients with pancreatic cancer. Int J Clin Oncol 15, 294–300, doi:10.1007/s10147-010-0066-5 (2010).
Karabagli, P., Ugras, S., Yilmaz, B. S. & Celik, C. The evaluation of reliability and contribution of frozen section pathology to staging endometrioid adenocarcinomas. Arch Gynecol Obstet 292, 391–397, doi:10.1007/s00404-015-3621-5 (2015).

No competing interests reported.

Download PDF

Journal Publication

published 03 Sep, 2021

Read the published version in Cancers →

Version 1

posted

You are reading this latest preprint version

Clinical Impact of Unexpected Para-Aortic Lymph Node Metastasis in Surgery for Resectable Pancreatic Cancer

Status:

Journal Publication

Version 1

Abstract

Figures

Introduction

Results

Baseline characteristics

Survival of patients with unexpected PALN

Other prognostic factors affecting overall survival

Surgical information including postoperative complications

Effects of overall lymph node status

Other medical information

Discussion

Materials And Methods

Patients

Study design

Statistical analysis

Declarations

References

Additional Declarations

Status:

Journal Publication

Version 1