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Originally published as Ann Surg Oncol Early Release 10.1245/ASO.2004.05.021 on March 15, 2004

Annals of Surgical Oncology 11:380-386 (2004)
© 2004 Society of Surgical Oncology
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ORIGINAL ARTICLES

Adenocarcinoma of the Duodenum: Importance of Accurate Lymph Node Staging and Similarity in Outcome to Gastric Cancer

Abeezar I. Sarela, MD, Murray F. Brennan, MD, Martin S. Karpeh, MD, David Klimstra, MD and Kevin C. P. Conlon, MD

From the Departments of Surgery (AIS, MFB, MSK, KCPC) and Pathology (DK), Memorial Sloan Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: Murray F. Brennan, MD, Department of Surgery, Memorial Hospital, 1275 York Ave., New York, NY 10021; Fax: 212-794-5854; E-mail: brennanm{at}mskcc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: This study examined prognostic discrimination by lymph node staging for duodenal adenocarcinoma and compared the nodal stage–specific survival with that associated with gastric antral adenocarcinoma.

Method: Prospectively maintained databases from 1983 to 2000 were reviewed to identify 137 patients with duodenal adenocarcinoma and 545 patients with gastric antral adenocarcinoma at a single institution.

Results: R0 resection was performed for 72 patients with duodenal cancer. At least 15 lymph nodes were retrieved in 34 cases (47%). Lymph node metastasis (pN+) was detected in 31 patients (43%). With median follow-up of 36 months, the pN category was an independently significant prognostic factor (pN0, 5-year disease-specific survival of 83%, vs. pN+, 56%; P = .03). The survival difference between pN0 and pN+ was pronounced in patients with >=15 nodes (100% vs. 47%, respectively; P = .01) but was lost in those with <15 nodes (75% vs. 64%; P = .5). For gastric antrum cancer, 331 patients had R0 resection, and >=15 nodes were retrieved in 256 cases (77%). Lymph node metastasis was detected in 157 cases (47%). For patients with >=15 nodes, 5-year survival with pN0 (87%) or pN+ (44%) was not significantly different from the corresponding categories for duodenal adenocarcinoma.

Conclusion: For duodenal adenocarcinoma, examination of >=15 regional lymph nodes improved prognostic discrimination by the pN category. With accurate nodal staging, pN0 was associated with excellent prognosis. With pN+, prognosis was similar to that for gastric antral adenocarcinoma.

Key Words: Antrum • Pancreatoduodenectomy • Periampullary • Prognosis • Stomach • Survival


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Adenocarcinoma of the duodenum is an uncommon disease.1,2 Up to 50% of duodenal adenocarcinomas occur in the vicinity of the ampulla of Vater,3 and these tumors are often grouped with other periampullary cancers. The prognosis for curatively resected duodenal adenocarcinoma (5-year survival, 60%)4 is substantially better, however, than that for cancer of the ampulla (46%),5 distal bile duct (27%),6 or head of pancreas (10%).7 It has been previously observed that the prognosis for duodenal cancer is, in fact, similar to that for gastric cancer.4,8 This observation has important clinical implications. The rarity of duodenal adenocarcinoma precludes clinical trials of adjuvant therapy specifically for this disease. Consequently, it is important to reliably establish the paradigm of identity so that adjuvant-therapy evidence for gastric cancer may reasonably be extrapolated to duodenal cancer.

For gastric adenocarcinoma, the pN category is an important prognostic indicator, and histopathological examination of >=15 regional lymph nodes is necessary for accurate nodal staging.9,10 Tumor location is also prognostically important.9,10 Cancers located at the gastroesophageal junction and in the proximal stomach are associated with significantly poor outcome in comparison to gastric antral cancers. We hypothesized that examination of >=15 nodes is important for accurate staging of duodenal adenocarcinoma as well and that the prognosis for this disease is similar to that for gastric antral adenocarcinoma. The present study aimed to evaluate the importance of examination of >=15 nodes on prognostic discrimination by pN category for duodenal adenocarcinoma and to compare nodal-stage-specific survival of patients with duodenal adenocarcinoma and gastric antral adenocarcinoma.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
A prospectively maintained database was used to identify patients with adenocarcinoma of the duodenum admitted to Memorial Hospital between 1983 and 2001. Some of these patients have been reported on previously.4,8 A similar database of gastric adenocarcinoma patients, for the period 1985 to 2001, was reviewed to identify patients with antral tumors. Clinical, operative, and pathological details were recorded for all patients. Clinical follow-up information was obtained at clinic visits and from physician records and phone calls to patients and/or their primary physicians.

Pathological staging of duodenal adenocarcinoma was conducted according to the 1997 American Joint Committee on Cancer (AJCC) system for small bowel cancer.11 The AJCC requires examination of at least six regional lymph nodes for assignment of the pN category (pN0 = no nodal metastasis and pN1 = nodal metastasis present). There is no further subdivision according to the number of involved nodes. Gastric antrum adenocarcinomas were staged according to the 1997 AJCC system for gastric cancer.11 Examination of at least 15 regional lymph nodes is required for assignment of the pN category (pN0 = no nodal metastasis; pN1 = metastasis in 1–6 nodes; pN2 = metastasis in 7–15 nodes; pN3 = metastasis in >15 nodes).

Statistical Analyses
The SPSS Version 10 statistical package (SPSS, Cary, NC) was used for analyses. Summary statistics are reported as median (range) or percentage and were compared with the Mann-Whitney U-test or {chi}2 test, as appropriate. Disease-specific survival was calculated from the date of operation to date of death of recurrent disease. Patients who were alive at the time of analysis or dead due to unrelated causes were censored at the date when last seen alive or date of death. The probability of disease-specific survival at 5 years and 10 years was estimated by the method of Kaplan-Meier, and log rank tests were used for comparison. For analysis of prognostic factors for disease-specific survival, a forward and backward stepwise Cox proportional hazards model was used. A P value of <.05 was considered statistically significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
One hundred thirty-seven patients with adenocarcinoma of the duodenum were identified. There were 75 men and 62 women, with a median age of 64 years (range, 34–89 years). Presenting symptoms comprised mainly abdominal pain (44%), weight loss (41%), and jaundice (31%). Seventy-two patients (53%) underwent potentially curative resection. The remainder underwent laparoscopy and/or laparotomy only, biliary bypass procedure, gastric bypass procedure, gastric and biliary bypass procedures, or no intervention.

The 72 patients who underwent potentially curative resection comprised 38 men and 34 women with a median age of 63 years (35–87 years). Pancreaticoduodenectomy was performed for 56 patients (78%) with tumors in the first or second portion of the duodenum, and segmental duodenal resection was performed for 16 patients (22%) with tumors in the third or fourth portion of the duodenum. There were two postoperative deaths (2.8%), both following pancreaticoduodenectomy.

All 72 resections were histopathologically confirmed as R0. Primary tumors had a median diameter of 4.0 cm (1.5–11.0), were poorly differentiated in 21 cases (29%), and were associated with a villous adenoma in 22 cases (31%). Nodal metastasis (pN1) was identified in 31 patients (43%). Patients with pN1 disease had a median of two involved lymph nodes (range, 1–17). There was a significant association between prevalence of pN1 disease and pT category (P < .001; Table 1). The median number of lymph nodes retrieved was 13 (0–70). No lymph node was retrieved from one segmental resection specimen. At least six lymph nodes were identified and examined in 59 cases (82%). Fifteen or more lymph nodes were identified in 34 cases (47%). The lymph node retrieval was significantly greater for tumors of the first or second portion of the duodenum as compared with tumors of the third or fourth portion (16 [8–24] vs. 9 [2–15]; P = .005). The prevalence of nodal metastasis in cases in which <15 nodes were retrieved was similar to that in cases in which >=15 nodes were retrieved (16 [42%] vs. 15 [44%]; P = .9).


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  		TABLE 1. Pathological staging of duodenal adenocarcinoma (all R0)
 
The median follow-up period was 36 months (2–205). Forty-four patients (61%) had no evidence of disease or had died of an unrelated cause at median follow-up of 51 months (1–185), and these included 19 patients who were alive for at least 5 years. Five patients (7%) were alive with recurrent disease at median follow-up of 16 months (4–177), including one 5-year survivor. Twenty-three patients (32%) died of recurrent disease, with median survival of 21 months (2–205), including six 5-year survivors. The disease-specific actuarial survival was 71% at 5 years and 54% at 10 years (Fig. 1). The operation had been performed prior to the year 1996 (yielding a minimum interval of 5 years to the date of conduct of this study) for 54 patients. With 26 actual 5-year survivors, the actual 5-year survival was 48%. On Cox regression analysis, only pN category and age were independent predictors of poor prognosis (Table 2). Gender, pT category, degree of differentiation, and extent of lymph node retrieval were not predictive of survival.



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  		FIG. 1. Disease-specific actuarial survival with duodenal adenocarcinoma and R0 resection (5-year survival, 71%; 10-year survival, 54%).

 

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  		TABLE 2. Univariate and multivariate analyses of prognostic factors following R0 resection of duodenal adenocarcinoma
 
The five-year actuarial survival with pN1 disease was significantly shorter than with pN0 disease (56% vs. 83% P = .03; Fig. 2). For patients with pN1 disease, the number of involved lymph nodes (one or two nodes vs. three or more nodes) did not influence survival (60% vs. 50%; P = .5). The difference in survival associated with pN1 disease or pN0 disease was particularly marked when >=15 lymph nodes had been examined (47% vs. 100%; P = .01; Fig. 3A). Five patients with pN1 died of recurrent disease, all within 38 months. Three patients with pN0 died of recurrent disease at 65 months, 86 months, and 206 months. In contrast, survival of patients with pN1 disease or pN0 disease was similar when <15 nodes had been examined (64% vs. 75%; P = .5; Fig. 3B). Survival of patients who had <15 lymph nodes retrieved was not significantly different from that of patients who had 15 or more nodes retrieved (5-year survival: 65% vs. 77%; P = .3).



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  		FIG. 2. Disease-specific actuarial survival with duodenal adenocarcinoma, stratified according to the pN category (pN0, 5-year survival of 83%, vs. pN1, 56%; P = .04).

 


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  		FIG. 3. Disease-specific actuarial survival with duodenal adenocarcinoma, stratified according to pN category with (A) examination of >=15 lymph nodes (pN0, 5-year survival of 100%, vs. pN1, 47%; P = .01) and (B) examination of <15 lymph nodes (pN0, 75%, vs. pN1, 64%; P = .5).

 
A total of 545 patients with adenocarcinoma of the gastric antrum were identified. There were 295 men and 250 women, with a median age of 67 years (27–96). R0 resection was performed for 331 patients (61%) and included a D2 or greater lymphadenectomy in 234 cases. The pT category was pTis for 9 (3%); pT1 for 92 (28%); pT2 for 114 (34%); pT3 for 108 (33%); and pT4 for 8 (2%). The pN category was pN0 for 174 (53%); pN1 for 105 (32%); pN2 for 40 (12%); and pN3 for 12 (3%). The median number of lymph nodes retrieved was 23 (16–32), and >=15 nodes were retrieved in 256 cases (77%). With examination of >=15 nodes, the pN category was pN0 for 126 (49%); pN1 for 80 (31%); pN2 for 38 (15%); and pN3 for 12 (5%). The median follow-up period was 31 months (1–188). When the pN category had been assigned by examination of >=15 nodes, the 5-year disease-specific actuarial survival was 87% with node-negative disease and 44% with node-positive (pN1–3) disease. With examination of >=15 nodes, there was no significant difference in survival characteristics of patients with node-negative duodenal cancer or node-negative gastric antral cancer (P = .9; Fig. 4A) Survival of patients with node-positive duodenal cancer or node-positive gastric antral cancer was also similar (P = .9; Fig. 4B).



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  		FIG. 4. Disease-specific actuarial survival with duodenal adenocarcinoma versus gastric antral adenocarcinoma, with examination of >=15 lymph nodes, for (A) node-negative disease (duodenal, 5-year survival of 100%, vs. gastric, 87%; P = .9) and (B) node-positive disease (duodenal, 47%, vs. gastric, 44%; P = .9).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
This study describes 137 patients with adenocarcinoma of the duodenum at a single institution. Seventy-two patients (53%) underwent resection with curative intent, and this proportion is consistent with previous data from Memorial Hospital4 and from other facilities (Table 3). Another 34% of patients underwent a palliative operation, and 13% of cases were managed nonoperatively. It is not surprising that studies that included only those patients who underwent exploratory laparotomy (and not cases that were managed nonoperatively) showed a higher resection rate (Table 3).


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  		TABLE 3. Series comprising at least 50 patients with duodenal adenocarcinoma reported since 1981
 
All resections were histopathologically confirmed as R0. At 5 years, the disease-specific actuarial survival was 71%. The survival was notably better than that in other reported series (Table 3). Such differences may be due partly to inclusion in previous reports of patients with R1 resection or death due to causes other than recurrent disease. It may also be speculated that better quality of clinical staging, with improved imaging techniques and laparoscopy, resulted in optimal patient selection and superior prognosis in the present series.

The pN category was an independently significant prognostic factor in the present study. Prognostic discrimination was particularly marked when the pN category had been assigned by examination of >=15 nodes. In contrast, the prognostic function was lost if <15 nodes had been examined. It may be that some previous studies (Table 3) failed to demonstrate the prognostic significance of nodal metastasis because the pN category had been assigned by examination of <15 nodes. Extensive studies have been conducted previously to confirm the threshold value of 15 lymph nodes for accurate determination of the N status of gastric adenocarcinoma.9,10 For any given threshold value, patients with a lymph node yield below the threshold are at risk for upstaging or the "stage migration" phenomenon.17 In addition, the probability of upstaging increases if higher threshold values are applied. Ultimately, the choice of a particular threshold value involves a balance between what is practically feasible and an acceptable probability of detecting nodal metastasis,18 and 15 nodes has been established by consensus in the AJCC.11 The rarity of duodenal adenocarcinoma precludes such a consensus process, and the threshold value of 15 nodes is extended from the data for gastric cancer. Studies on gastric adenocarcinoma have shown that lymph node retrieval from the resected specimen is dependent on the extent of lymphadenectomy as well as the protocol and technique of retrieval.19 Similar considerations are likely to apply to duodenal adenocarcinoma.

In the present study, the pN0 category probably comprises truly node-negative patients only in the subgroup in which >=15 nodes were examined. The favorable biological characteristics are reflected in the prolonged disease-specific survival of this subgroup. In contrast, the pN0 category is likely to be "contaminated" with undetected pN1 (false-negative) cases in the subgroup with <15 nodes. These false-negative cases may undergo stage migration to the pN1 category if >=15 nodes were examined. Although the proportion of patients with nodal metastasis was similar in the subgroups with <15 nodes or 15 or more nodes, this does not disprove the stage-migration hypothesis. In gastric adenocarcinoma, too, examination of 15 or more nodes resulted in increased survival for each of the N categories, without any significant change in the stage distribution.10

Old age (>60 years) was another significantly adverse prognostic factor in the present study. This association has not been previously reported for duodenal adenocarcinoma. The pT category was not a significant prognostic factor in the present series of duodenal adenocarcinoma. This observation is contrary to some prior reports.15,20 It is likely that the present study had insufficient power to detect the prognostic value of the pT category, mainly because of the small proportion of patients with pT1 or pT2 tumors.

Survival characteristics of patients who had undergone R0 resection of distal gastric adenocarcinoma were also examined. With assignment of the pN category by examination of >=15 nodes, survival for pN0 duodenal adenocarcinoma or pN0 gastric adenocarcinoma was excellent. With node-positive disease, survival with either duodenal cancer or gastric antral cancer was almost identical. For node-positive duodenal cancer, there were only three patients with 7 to 15 metastatic lymph nodes (analogous to pN2 category for gastric cancer) and two patients with >15 metastatic lymph nodes (analogous to pN3 category for gastric cancer). Consequently, substratification of node-positive patients with duodenal cancer was not conducted. The present data corroborate previous observations that the prognoses of duodenal cancer and gastric cancer are similar.4,8 Because proximally located gastric adenocarcinomas are clearly associated with a worse prognosis,9,10 the present study restricted comparison of duodenal cancer to gastric antral cancer.

In conclusion, following R0 resection of duodenal adenocarcinoma, examination of >=15 lymph nodes resulted in improved prognostic discrimination by the pN category. Such improvement in prognostic accuracy was most likely because of a stage-migration effect. Patients with accurately staged pN0 duodenal adenocarcinoma had excellent survival rates and are highly unlikely to benefit from adjuvant therapy. In contrast, pN1 disease was associated with 5-year survival of 47%, very similar to that for node-positive gastric antral adenocarcinoma. Patients with node-positive gastric adenocarcinoma may benefit from adjuvant 5-fluorouracil/leucovorin and radiation therapy.21 The rarity of duodenal adenocarcinoma precludes a clinical trial of adjuvant therapy specifically for this disease. The present data suggest consideration of adjuvant therapy for patients who have undergone potentially curative resection of duodenal adenocarcinoma and are at high-risk for recurrence.12,14,16


   ACKNOWLEDGMENTS
 
The authors are grateful to Ms. Helen Thorpe, Medical Statistician, Clinical Trials and Research Unit, University of Leeds, UK, for review of the manuscript and valuable advice.


   FOOTNOTES
 
This article was presented in part as a poster at the Annual Meeting of the Society of Surgeons of the Alimentary Tract, Digestive Diseases Week, May 2002, San Francisco, California.

For patients with R0 resection of duodenal adenocarcinoma and examination of >=15 regional lymph nodes, the prognosis for node-negative disease was excellent (5-year disease-specific survival, 100%). With node-positive disease, survival of duodenal adenocarcinoma (47%) was similar to that of gastric antral adenocarcinoma (44%).

Received for publication May 21, 2003. Accepted for publication December 21, 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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