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Outcomes of octogenarians undergoing gastrectomy performed for malignancy
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Outcomes of octogenarians undergoing gastrectomy performed for malignancy Annabelle Teng, MD,a,* Geoffrey Bellini, MD,a Erica Pettke, MD,a Michael Passeri, MD,a David Y. Lee, MD,c Keith Rose, MD,b Anton J. Bilchik, MD,c and Fadi Attiyeh, MD, FACSa a
Department of Surgery, Mount Sinai St. Luke’s Roosevelt Hospital, New York, New York Department of Critical Care, Mount Sinai St. Luke’s Roosevelt Hospital, New York, New York c Department of Surgical Oncology, John Wayne Cancer Institute, Santa Monica, California b
article info
abstract
Article history:
Background: Studies on perioperative outcomes of octogenarians with gastric cancer are
Received 13 January 2016
limited by small sample size. Our aim was to determine the outcomes of gastrectomy and
Received in revised form
the variation of treatments associated with advanced age (80 y).
25 June 2016
Methods: The National Surgical Quality Improvement Program database was queried from
Accepted 3 August 2016
2005 to 2011. Patients who underwent gastrectomy for malignancy were identified using
Available online 12 August 2016
International Classification of Diseases, Ninth Revision and Current Procedural Terminology codes.
Keywords:
Results: Of 2591 cases, 487 patients were octogenarians (80) and 2104 were non-
Gastric cancer
octogenarians (<80). Overall, 4.9% of patients had disseminated cancer. Octogenarians had
Gastrectomy
higher 30-d mortality (7.2% versus 2.5%, P < 0.01) and more major complications (31.4%
Elderly
versus 25.5%, P < 0.01), though fewer octogenarians underwent total gastrectomy (24.0%
Octogenarian
versus 43.2%, P < 0.01) and extended lymphadenectomy (10.1% versus 17.4%, P < 0.01) than
American College of Surgeons Na-
the nonoctogenarian cohort. On multivariate analysis, age 80 y was associated with major
tional Surgical Quality Improve-
complications (OR, 1.3; 95% CI, 1.03-1.6; P ¼ 0.03) and increased mortality (OR, 3.0; 95% CI,
ment Program (ACS-NSQIP)
1.9-4.9; P < 0.01). Conclusions: Advanced age (80 y) was associated with worse outcomes in patients undergoing gastrectomy for malignancy. Therefore, careful staging is necessary to reduce unnecessary operations in this population. Furthermore, surgeons must place greater attention on optimizing the octogenarian population before surgery. ª 2016 Elsevier Inc. All rights reserved.
Introduction While the incidence of gastric cancer has been decreasing in the United States, it remains the second leading cause of cancer mortality worldwide.1 Although early screening, combined with advances in modern surgical therapy, chemotherapeutic agents and radiotherapy have improved survival
for patients with gastric cancer in the developed nations in the East, 5-y survival for newly diagnosed gastric cancer in the United States remains dismal at 29.3%.2-6 In 2015, there were 24,590 new cases of gastric cancer diagnosed in the United States and 10,720 deaths.6 As the population ages, more elderly patients will undergo gastrectomy for treatment of gastric cancer. Gastrectomy performed
* Corresponding author. Department of Surgery, Mount Sinai St Luke’s Roosevelt Hospital Center, 1000 10th Ave Suite 2B, New York, NY 10019. Tel.: þ1 (212) 523 6970; fax: þ1 (212) 523 6495. E-mail address: [email protected] (A. Teng). 0022-4804/$ e see front matter ª 2016 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jss.2016.08.020
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for gastric cancer in the United States carries a high perioperative morbidity and mortality.7 Many studies looking at the outcomes of “elderly” patients have used a cutoff age of 70 y. This is, however, very close to the median age of diagnosis, which is 69 in the current era.8-10 Furthermore, most series examining the perioperative outcomes of octogenarians are limited in size.11,12 Therefore, we examined the American College of Surgeon’s National Surgical Quality Improvement Program participant user file (ACS-NSQIP PUF) to examine the perioperative outcomes of octogenarians undergoing gastrectomy for malignancy. Our aim was to determine the 30d mortality and morbidity of this patient population and to study the variation of treatments associated with advanced age (80 y).
Methods After obtaining exemption from our institutional review board, we performed a review of the ACS-NSQIP PUF database. The ACS-NSQIP PUF database is a risk adjusted outcomesbased program designed to measure and improve the quality of surgical care. The program collects data on over 130 preoperative, intraoperative, and postoperative clinical variables. In addition, 30-d postoperative mortality and morbidity data are collected in the database. Currently, there are over 300 hospitals that participate in this program.13 The ACS-NSQIP PUF database was queried from 2005 to 2011 for gastrectomy performed for malignancy. Current Procedural Terminology (CPT) codes for subtotal and total gastrectomies (43620-43622, 43631-43634) were used in conjunction with International Classification of Diseases, Ninth Revision codes (151.x) to identify all patients who underwent gastrectomy for malignancy. Secondary CPT codes were used to identify additional organ resections, and CPT code 38,747 was used to identify extended lymphadenectomy defined as regional lymph node dissection including celiac, gastric, portal, peripancreatic with or without the para-aortic, and vena cava regions. All emergent cases were excluded from our analysis. Clinically relevant preoperative, intraoperative, and postoperative events including 30-day mortality and complications were noted and reviewed. Major complications were defined as occurrence of one of the following events: superficial and deep organ space infection, wound dehiscence, reintubation, prolonged ventilation, pulmonary embolism, acute renal failure requiring dialysis, cerebral vascular accident, coma greater than 24 h, cardiac arrest, myocardial infarction, need for transfusion greater than four units postoperatively, sepsis, septic shock, and return to the operating room. All clinical factors in the ACSNSQIP database are defined in the user guide.14 Patients were grouped into octogenarians (80 y) and nonoctogenarians (<80 y). Categorical variables were analyzed between the two groups by chi-square test and continuous variables with Student’s t-test and ManneWhitney U test where appropriate. In addition, multivariate stepwise logistic regression was used to evaluate advanced age as an independent variable on occurrence of mortality and major postoperative complications. We also studied other clinically relevant preoperative variables to
generate odds ratios for factors associated with mortality and occurrence of major complications. All statistical analyses were performed on SPSS for Windows version 23 (SPSS Inc, Chicago, IL).
Results Patient demographics and characteristics We identified 2591 gastrectomies performed for malignancy in the NSQIP database. The average age of the cohort was 66.6 13.7 y. Of these patients, 487 were octogenarians (mean age, 83.8 3.1 y). A significantly higher proportion of octogenarians had cardiac, pulmonary, and neurologic comorbidities compared to nonoctogenarians. Furthermore, a higher proportion of octogenarians had American Society of Anesthesiology III/IV classifications, worse functional status, and lower average body mass index compared to nonoctogenarians. Overall, 4.9% of the patients who underwent gastrectomy had a diagnosis of disseminated cancer. However, the proportion of patients with disseminated cancer, the sex profile, and preoperative weight loss were similar between the two groups (Table 1).
Treatment characteristics A significantly lower proportion of octogenarians underwent radiation therapy (0.8% versus 3.2%, P ¼ 0.004) and chemotherapy (1.6% versus 7.3%, P < 0.001) before gastrectomy compared to nonoctogenarians. However, the rate of a prior surgery within 30-d before gastrectomy was similar between the two groups (0.8% versus 1.4%, P ¼ 0.360). Octogenarians underwent less extensive operations compared to nonoctogenarians. Only 24.0% of octogenarians underwent total gastrectomy compared to 43.2% of nonoctogenarians (P < 0.001). In addition, fewer octogenarians underwent extended lymphadenectomy (10.1% versus 17.4%, P < 0.001). The rates of additional organ resection were similar between the two groups except for pancreatic resection, which was greater in the nonoctogenarian group (2.8% versus 1.6%, P < 0.042). Additional operative details are summarized in Table 2.
Outcomes The rate of 30-d mortality in this overall cohort was 3.4%, and the rate of major complications was 26.5%. The 30-d mortality rate in octogenarians was nearly 3 times that of nonoctogenarians (7.2% versus 2.5%, P < 0.001). In addition, octogenarians experienced significantly higher rates of major complications compared to nonoctogenarians (31.4% versus 25.5% P ¼ 0.008), even with less extensive operations. Specifically, in descending order, the rates of pulmonary complications, septic shock, and cardiac complications were significantly higher in octogenarians. The rates of pneumonia and unplanned intubation were almost twice as high in the octogenarian group. However, the average time to death and the length of stay were similar between the two groups (Table 3).
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teng et al gastrectomy in octogenarians
Table 1 e Comparison of demographics and comorbidities between octogenarians and nonoctogenarians. Characteristics
Age (mean)
Female Disseminated cancer
0.752
1235 (58.7)
273 (56.1)
History of TIA
51 (2.4)
35 (7.2)
<0.001
868 (41.3)
214 (43.9)
53 (2.5)
18 (3.7)
0.152
105 (5.0)
22 (4.5)
History of CVA and/or neurologic deficit History of CVA and/or no neurologic deficit
34 (1.6)
20 (4.1)
0.001
0.499
0.663 <0.001
88 (18.1) 349 (71.7)
IV
106 (5.0)
49 (10.1)
4 (0.1)
Diabetes Chronic steroid use <0.001
2020 (96.0)
441 (90.6)
75 (3.6)
40 (8.2)
9 (0.4)
6 (1.2)
CNS comorbidities
Endocrine history
1 (0.2)
Functional status (before surgery)
Ascites
ETOH (2 drinks/d 2 wk before surgery)
2042 (97.1)
471 (96.7)
0.694
26.7 6.4
25.1 5.2
0.001
>10% Weight loss in last 6 mo
359 (17.1)
70 (14.4)
0.150
Do not resuscitate status (yes)
8 (0.4)
4 (0.8)
0.196
381 (18.1)
94 (19.3)
0.540
34 (1.6)
11 (2.3)
0.328
Gastrointestinal history
Smoker (within 1 y)
Transfer status
BMI (mean)
2 (0.4)
0.001
742 (35.3)
Admitted from home
11 (0.5)
83.8 3.1
1252 (59.5)
Totally dependent
Preoperative dialysis dependence
62.6 11.9
III
Partially dependent
P value
P value
I-II
Independent
Aged 80 y, (n ¼ 487), n (%)
Aged 80 y, (n ¼ 487), n (%)
ASA class
Unknown
Aged <80 y, (n ¼ 2104), n (%)
Aged <80 y, (n ¼ 2104), n (%)
Gender Male
Table 1 e (continued ) Characteristics
13 (0.6)
5 (1.0)
0.328
455 (21.6)
25 (5.1)
<0.001
72 (3.4)
11 (2.3)
0.189
ASA class ¼ American Society of Anesthesiology Classification System; BMI ¼ body mass index; CHF ¼ congestive heart failure; CNS ¼ central nervous system; COPD ¼ chronic obstructive pulmonary disease; CVA ¼ cerebral vascular accident; ETOH ¼ alcohol abuse; heme ¼ hematology; HTN ¼ hypertension; meds ¼ medications; MI ¼ myocardial infarction; onc ¼ oncology; PCI ¼ percutaneous coronary intervention; TIA ¼ transient ischemic attack.
Preoperative comorbidities Cancer history (heme/ onc) Radiotherapy (<90 d)
68 (3.2)
4 (0.8)
0.004
Prior chemotherapy (<30 d)
154 (7.3)
8 (1.6)
<0.001
83 (3.9)
28 (5.7)
0.076
Bleeding disorders Cardiovascular history HTN (requiring meds)
<0.001
1094 (52.0)
376 (77.2)
MI (within 6 mo)
13 (0.6)
4 (0.8)
0.616
CHF (within 30 d before surgery)
16 (0.8)
7 (1.4)
0.151
Angina (in 1 mo before surgery)
13 (0.6)
9 (1.8)
0.008
Cardiac surgery
118 (5.6)
62 (12.7)
<0.001
PCI
136 (6.5)
61 (12.5)
<0.001
35 (1.7)
15 (3.1)
250 (11.9)
82 (16.8)
No dyspnea
1854 (88.1)
405 (83.2)
Severe COPD
100 (4.8)
42 (8.6)
4 (0.2)
1 (0.2)
History of distal revascularization Pulmonary history Dyspnea at rest/exertion
0.041 0.003
Discussion
Renal history Preoperative acute renal failure
On multivariate analysis, age 80 y was an independent risk factor associated with death (OR, 3.0; 95% CI, 1.9-4.9; P ¼ 0.003). The strongest predictor of death was performance of concomitant small bowel resection (OR, 4.6; 95% CI, 2.0-10.7; P < 0.001) followed by splenectomy and colon resection. Additional factors associated with mortality include total gastrectomy, pre-operative weight loss, dyspnea, and functional dependence (Table 4). Extended lymphadenectomy was not associated with increased mortality (OR, 1.0, 95% CI, 0.81.3, P ¼ 0.797). Age 80 y was also an independent risk factor associated with the occurrence of major complications (OR, 1.3; 95% CI, 1.03-1.6; P ¼ 0.025) on multivariate analysis. Other factors associated with the occurrence of major complications include total gastrectomy, additional organ resection, preoperative dialysis, and functional dependence (Table 5). Extended lymphadenectomy was not associated with an increase in morbidity (OR, 0.97; 95% CI, 0.76-1.23; P ¼ 0.790).
0.945 (continued)
Despite the improvement in perioperative care and modern surgical technique, gastrectomies performed for malignancy in the United States carry high perioperative morbidity and mortality. Our analysis serves as the largest study to date of octogenarians undergoing gastrectomy. The octogenarian
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Table 2 e Treatment details.
Table 3 e Postoperative adverse events.
Characteristics
Aged < 80 y, (n ¼ 2104), n (%)
Aged 80 y, (n ¼ 487), n (%)
P value
Characteristics
Anesthesia time (min)
300.3 120.2
265.0 107.2
<0.001
Death
Surgery time (min)
237.1 104.0
201.0 90.2
0.003
Preoperative treatment Prior surgery (within 30 d)
29 (1.4)
4 (0.8)
0.360
Radiotherapy (<90 d)
68 (3.2)
4 (0.8)
0.004
Prior chemotherapy (<30 d)
154 (7.3)
8 (1.6)
<0.001
Total gastrectomy Partial gastrectomy
908 (43.2)
117 (24.0)
1196 (56.8)
370 (76.0)
<0.001
Extended lymphadenectomy
366 (17.4)
49 (10.1)
Pancreatic resection
39 (2.8)
20 (1.6)
Hepatic resection Splenectomy
28 (1.3)
4 (0.8)
<0.001 0.042 0.359
113 (5.4)
18 (3.7)
0.129
Esophagectomy
17 (0.8)
3 (0.6)
0.663
Small bowel resection
62 (2.9)
12 (2.5)
0.564
Colectomy
60 (2.9)
15 (3.1)
0.786
Intraoperative or postoperative transfusion (yes)
143 (6.8)
44 (9.0)
0.083
Return to operating room
173 (8.2)
29 (6.0)
0.093
P value
<0.001
53 (2.5)
35 (7.2)
12.5 8.2
12.8 7.6
0.867
Days to discharge
10.8 8.5
11.9 9.5
0.020
Return to operating room
173 (8.2)
29 (6.0)
0.093
Major complications
537 (25.5)
153 (31.4)
0.008
MI
19 (0.9)
10 (2.1)
0.030
Cardiac arrest
27 (1.3)
13 (2.7)
0.025
Cardiac complications
Pulmonary complications 121 (5.8)
53 (10.9)
<0.001
Unplanned intubation
97 (4.6)
45 (9.2)
<0.001
Ventilator dependence > 48 h
107 (5.1)
31 (6.4)
0.257
Pulmonary emboli
25 (1.2)
7 (1.4)
0.654
Deep venous thrombosis
29 (1.4)
7 (1.4)
0.994
Acute renal failure requiring dialysis
14 (0.7)
7 (1.4)
0.087
Progressive renal insufficiency
13 (0.6)
3 (0.6)
0.996
Cerebral vascular accident with deficit
8 (0.4)
4 (0.8)
0.196
Coma >24 h
6 (0.2)
2 (0.4)
0.338
158 (7.5)
29 (6.0)
0.232
82 (3.9)
35 (7.2)
0.002
Renal complications
Neurologic complications
Infectious complications Sepsis Septic shock
cohort underwent less extensive operations compared to nonoctogenarians as evidenced by a lower rate of total gastrectomy (24.0 versus 43.2%) and extended lymphadenectomy (10.1% versus 17.4%). Despite less extensive surgical procedures, octogenarians still experienced a higher rate of complications and mortality compared to nonoctogenarians. Our study is noteworthy in that extended lymphadenectomy was not an independent predictor of worse outcomes. In the Dutch gastric cancer trial, extended lymphadenectomy (D2) resulted in significantly higher postoperative mortality compared to the limited lymphadenectomy (D1) offsetting any potential long-term effect in survival.15 However, in the Dutch trial, splenectomy was routinely performed as part of the D2 dissection. In our study, extended lymphadenectomy without additional organ resection did not increase postoperative mortality or morbidity. This suggests that in the modern surgical era, extended lymphadenectomy can be safely performed. While the ACS-NSQIP database, does not explicitly define extended lymphadenectomy as D1, D2, or state the number of nodes harvested, it describes a regional lymphadenectomy which goes well beyond harvesting just the perigastric nodes (regional lymph node dissection including celiac, gastric, portal, peripancreatic with or without the para-aortic, and vena cava regions). Furthermore, octogenarians received
Aged 80 y, (n ¼ 487), n (%)
Days to death
Pneumonia
Additional procedures performed
Aged < 80 y, (n ¼ 2104), n (%)
Urinary tract infection Superficial wound infection Deep incisional wound infection Wound disruption Organ space infection
84 (4.0)
27 (5.5)
0.128
119 (5.7)
29 (6.0)
0.798
36 (1.7)
3 (0.6)
0.074
35 (1.7)
6 (1.2)
0.492
146 (6.9)
26 (5.3)
0.201
MI ¼ myocardial infarction.
significantly less preoperative chemotherapy and radiation therapy. Previous studies with smaller patient populations have shown increased morbidity and mortality for octogenarians undergoing gastrectomy.12,15 However, our study is the first to show in such a large cohort that age 80 y itself confers a significantly higher risk for 30-d perioperative complications and a three times higher 30-d mortality risk on multivariate analysis. These results suggest that surgeons need to place greater emphasis on preparing and optimizing the octogenarian population before heading to the operating room. In a recent study, however, Ghignone et al. surveyed 251 surgical members of either the European Society of Surgical Oncology or the Society of Surgical Oncology and found that the majority of surgeons do not consider age as a potential limitation to
teng et al gastrectomy in octogenarians
Table 4 e Multivariate analysis of preoperative factors associated with an occurrence of a major complication. Prognostic factors Age 80 y
Adjusted, OR (95% CI) 1.3 (1.03-1.6)
P value 0.025
Total gastrectomy
1.6 (1.3-1.9)
<0.001
Colon resection
2.7 (1.7-4.5)
<0.001
Pancreatic resection
2.3 (1.3-4.2)
0.004
Splenectomy
1.6 (1.1-2.3)
0.019
Preoperative dialysis
3.4 (1.04-11.3)
0.042
CI ¼ confidence interval; OR ¼ odds ratio.
surgery. They also found that only about one-third of those surgeons coordinate their patient’s care with a geriatrician.16 Another recent study by Sakurai et al.17 examined the preoperative nutritional status of 594 patients with gastric cancer that underwent gastrectomy and found that 5-y survival was significantly worse in the patient cohort with a lower preoperative nutritional status. Combined with the current literature, our results strongly suggest that further research into the optimization and the multidisciplinary coordination of preoperative care of the octogenarian population is necessary in an attempt to improve postoperative morbidity and mortality for gastrectomy. Our examination of the ACS-NSQIP database also shows that there may be room for improvement in patient selection in both patient cohorts. Approximately 5% of the patients in the ACS-NSQIP database who underwent elective gastrectomy for malignancy had disseminated cancer, with no difference between octogenarians and nonoctogenarians (4.5% versus 5.0%). The current National Cancer Comprehensive guideline states that carcinomas should be considered unresectable in the case of positive peritoneal cytology (M1 disease) even in the absence of gross peritoneal disease and that gastric resection should be reserved for palliation of symptoms (obstruction or uncontrollable bleeding).18 In a retrospective review of 1241 patients at the Memorial Sloan Kettering Cancer Center who underwent laparoscopy with peritoneal washing for gastric cancer, 291 (23%; 198 with visible metastatic disease and 93 without gross disease but positive
5
cytology) patients had metastatic disease.19 Therefore, it is possible that the use of diagnostic laparoscopy with peritoneal lavage as a separate staging procedure may have helped to avoid unnecessary gastrectomies in patients with disseminated cancer. Another limitation of this study is that we were unable to determine whether gastrectomy was performed open or laparoscopic. Currently, outside of high-volume centers, laparoscopic resection of gastric cancer is not commonly performed in the United States.17 However, groups with extensive experience from both the West (United States and Europe) and the East (Japan, Korea, and Taiwan) have shown that in carefully selected patients, a minimally invasive surgical approach can improve perioperative outcomes with equivalent oncologic outcomes.20-26 Other studies examining the benefits of minimally invasive surgery for elderly patients undergoing different anatomic resections have also been performed. For example, Frasson et al. performed a randomized study comparing the effects of open and laparoscopic colorectal resections in patients <70 and patients 70. They concluded that laparoscopy in this case improved short-term outcomes for the elderly cohort more so than in the younger population.27 Further study into the laparoscopic approach for gastrectomy in the octogenarian population is warranted.
Conclusions To our knowledge, this is the largest series of octogenarians undergoing gastrectomy for malignancy in the literature. Perioperative morbidity and mortality of gastrectomy performed for malignancy is high, especially for octogenarians, in the United States. However, extended lymphadenectomy without additional organ resection did not increase morbidity or mortality in either patient cohort. Given such a high rate of perioperative morbidity and mortality, preoperative nutritional optimization as well as coordination of care for octogenarians undergoing gastrectomy may be an avenue to decrease their postoperative complications. Further research into preoperative care for octogenarians is necessary. Also, careful patient selection is paramount to avoid the potential complications of gastrectomy in patients who will not benefit from the operation. In our study, we found that nearly 5% of patients had disseminated cancer. Careful staging of these patients may reduce unnecessary operations.
Table 5 e Multivariate analysis of preoperative factors associated with 30-d mortality. Prognostic factors Age 80 y
Adjusted, OR (95% CI) 3.0 (1.9-4.9)
P value 0.003
Total gastrectomy
2.0 (1.3-3.3)
0.003
Colonic resection
3.2 (1.4-7.7)
0.007
Small bowel resection
4.6 (2.0-10.7)
<0.001
Splenectomy
3.5 (1.8-6.8)
<0.001
Weight loss
1.8 (1.1-3.1)
0.018
Dyspnea
1.8 (1.04-3.1)
0.036
Functionally dependent
2.7 (1.4-5.3)
0.003
CI ¼ confidence interval; OR ¼ odds ratio.
Acknowledgment The American College of Surgeon’s National Surgical Quality Improvement Program and the hospitals participating in the ACS-NSQIP are the source of the data used herein: they have not verified and are not responsible for the statistical validity of the data analysis or the conclusions derived by the author. Authors’ contributions: Conception and design were done by D.Y.L., A.T., A.J.B., and F.A. Analysis and interpretation and drafting of the article were executed by D.Y.L., A.T., G.B., M.P., E.P., and K.R. Data collection was carried out by D.Y.L., A.T.,
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and E.P. Critical revision was done by A.J.B., K.R., F.A., G.B., D.Y.L., and A.T. 14.
Disclosure 15.
The authors report no proprietary or commercial interest in any product mentioned or concept discussed in this article. 16.
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specifics/data-collection-analysis-and-reporting/. Accessed May 31, 2012. American College of Surgeons. Acs NSQIP Userguide for the 2010 participant Use data file. Chicago, IL: American College of Surgeons; 2011. Hartgrink HH, van de Velde CJ, Putter H, et al. Extended lymph node dissection for gastric cancer: who may benefit? Final results of the randomized Dutch gastric cancer group trial. J Clin Oncol. 2004;22:2069e2077. Ghignone F, van Leeuwen BL, Montroni I, et al. The assessment and management of older cancer patients: a SIOG surgical task force survey on surgeons’ attitudes. Eur J Surg Oncol. 2016;42:297e302. Sakurai K, Ohira M, Tamura T, et al. Predictive potential of preoperative nutritional status in long-term outcome projections for patients with gastric cancer. Ann Surg Oncol. 2016;23:525e533. Network NCC. NCCN Clinical Pracie Guldeins in Oncolgoy Gastric Cancer (Version 3.2015). Available at: http://nccn.org/ professionals/physicians_gls/PDF/gastric.pdf. Accessed September 22, 2015. Songun I, Putter H, Kranenbarg EM, Sasako M, van de Velde CJ. Surgical treatment of gastric cancer: 15-year followup results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol. 2010;11:439e449. Strong VE. Laparoscopic resection for gastric carcinoma: Western experience. Surg Oncol Clin N Am. 2012;21:141e158. Strong VE, Devaud N, Allen PJ, Gonen M, Brennan MF, Coit D. Laparoscopic versus open subtotal gastrectomy for adenocarcinoma: a case-control study. Ann Surg Oncol. 2009;16:1507e1513. Ding J, Liao GQ, Liu HL, Liu S, Tang J. Meta-analysis of laparoscopy-assisted distal gastrectomy with D2 lymph node dissection for gastric cancer. J Surg Oncol. 2012;105:297e303. Kim W, Kim HH, Han SU, et al. Decreased morbidity of laparoscopic distal gastrectomy compared with open distal gastrectomy for stage I gastric Cancer: short-term outcomes from a Multicenter Randomized Controlled trial (KLASS-01). Ann Surg. 2016;263:28e35. Haverkamp L, Weijs TJ, van der Sluis PC, van der Tweel I, Ruurda JP, van Hillegersberg R. Laparoscopic total gastrectomy versus open total gastrectomy for cancer: a systematic review and meta-analysis. Surg Endosc. 2013;27:1509e1520. Jeong O, Jung MR, Kim GY, Kim HS, Ryu SY, Park YK. Comparison of short-term surgical outcomes between laparoscopic and open total gastrectomy for gastric carcinoma: case-control study using propensity score matching method. J Am Coll Surg. 2013;216:184e191. Xiong JJ, Nunes QM, Huang W, et al. Laparoscopic vs open total gastrectomy for gastric cancer: a meta-analysis. World J Gastroenterol. 2013;19:8114e8132. Frasson M, Braga M, Vignali A, et al. Benefits of laparoscopic colorectal resection are more pronounced in elderly patients. Dis Colon Rectum. 2008;51:296e300.
Available online at www.sciencedirect.com
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Outcomes of octogenarians undergoing gastrectomy performed for malignancy Annabelle Teng, MD,a,* Geoffrey Bellini, MD,a Erica Pettke, MD,a Michael Passeri, MD,a David Y. Lee, MD,c Keith Rose, MD,b Anton J. Bilchik, MD,c and Fadi Attiyeh, MD, FACSa a
Department of Surgery, Mount Sinai St. Luke’s Roosevelt Hospital, New York, New York Department of Critical Care, Mount Sinai St. Luke’s Roosevelt Hospital, New York, New York c Department of Surgical Oncology, John Wayne Cancer Institute, Santa Monica, California b
article info
abstract
Article history:
Background: Studies on perioperative outcomes of octogenarians with gastric cancer are
Received 13 January 2016
limited by small sample size. Our aim was to determine the outcomes of gastrectomy and
Received in revised form
the variation of treatments associated with advanced age (80 y).
25 June 2016
Methods: The National Surgical Quality Improvement Program database was queried from
Accepted 3 August 2016
2005 to 2011. Patients who underwent gastrectomy for malignancy were identified using
Available online 12 August 2016
International Classification of Diseases, Ninth Revision and Current Procedural Terminology codes.
Keywords:
Results: Of 2591 cases, 487 patients were octogenarians (80) and 2104 were non-
Gastric cancer
octogenarians (<80). Overall, 4.9% of patients had disseminated cancer. Octogenarians had
Gastrectomy
higher 30-d mortality (7.2% versus 2.5%, P < 0.01) and more major complications (31.4%
Elderly
versus 25.5%, P < 0.01), though fewer octogenarians underwent total gastrectomy (24.0%
Octogenarian
versus 43.2%, P < 0.01) and extended lymphadenectomy (10.1% versus 17.4%, P < 0.01) than
American College of Surgeons Na-
the nonoctogenarian cohort. On multivariate analysis, age 80 y was associated with major
tional Surgical Quality Improve-
complications (OR, 1.3; 95% CI, 1.03-1.6; P ¼ 0.03) and increased mortality (OR, 3.0; 95% CI,
ment Program (ACS-NSQIP)
1.9-4.9; P < 0.01). Conclusions: Advanced age (80 y) was associated with worse outcomes in patients undergoing gastrectomy for malignancy. Therefore, careful staging is necessary to reduce unnecessary operations in this population. Furthermore, surgeons must place greater attention on optimizing the octogenarian population before surgery. ª 2016 Elsevier Inc. All rights reserved.
Introduction While the incidence of gastric cancer has been decreasing in the United States, it remains the second leading cause of cancer mortality worldwide.1 Although early screening, combined with advances in modern surgical therapy, chemotherapeutic agents and radiotherapy have improved survival
for patients with gastric cancer in the developed nations in the East, 5-y survival for newly diagnosed gastric cancer in the United States remains dismal at 29.3%.2-6 In 2015, there were 24,590 new cases of gastric cancer diagnosed in the United States and 10,720 deaths.6 As the population ages, more elderly patients will undergo gastrectomy for treatment of gastric cancer. Gastrectomy performed
* Corresponding author. Department of Surgery, Mount Sinai St Luke’s Roosevelt Hospital Center, 1000 10th Ave Suite 2B, New York, NY 10019. Tel.: þ1 (212) 523 6970; fax: þ1 (212) 523 6495. E-mail address: [email protected] (A. Teng). 0022-4804/$ e see front matter ª 2016 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jss.2016.08.020
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j o u r n a l o f s u r g i c a l r e s e a r c h j a n u a r y 2 0 1 7 ( 2 0 7 ) 1 e6
for gastric cancer in the United States carries a high perioperative morbidity and mortality.7 Many studies looking at the outcomes of “elderly” patients have used a cutoff age of 70 y. This is, however, very close to the median age of diagnosis, which is 69 in the current era.8-10 Furthermore, most series examining the perioperative outcomes of octogenarians are limited in size.11,12 Therefore, we examined the American College of Surgeon’s National Surgical Quality Improvement Program participant user file (ACS-NSQIP PUF) to examine the perioperative outcomes of octogenarians undergoing gastrectomy for malignancy. Our aim was to determine the 30d mortality and morbidity of this patient population and to study the variation of treatments associated with advanced age (80 y).
Methods After obtaining exemption from our institutional review board, we performed a review of the ACS-NSQIP PUF database. The ACS-NSQIP PUF database is a risk adjusted outcomesbased program designed to measure and improve the quality of surgical care. The program collects data on over 130 preoperative, intraoperative, and postoperative clinical variables. In addition, 30-d postoperative mortality and morbidity data are collected in the database. Currently, there are over 300 hospitals that participate in this program.13 The ACS-NSQIP PUF database was queried from 2005 to 2011 for gastrectomy performed for malignancy. Current Procedural Terminology (CPT) codes for subtotal and total gastrectomies (43620-43622, 43631-43634) were used in conjunction with International Classification of Diseases, Ninth Revision codes (151.x) to identify all patients who underwent gastrectomy for malignancy. Secondary CPT codes were used to identify additional organ resections, and CPT code 38,747 was used to identify extended lymphadenectomy defined as regional lymph node dissection including celiac, gastric, portal, peripancreatic with or without the para-aortic, and vena cava regions. All emergent cases were excluded from our analysis. Clinically relevant preoperative, intraoperative, and postoperative events including 30-day mortality and complications were noted and reviewed. Major complications were defined as occurrence of one of the following events: superficial and deep organ space infection, wound dehiscence, reintubation, prolonged ventilation, pulmonary embolism, acute renal failure requiring dialysis, cerebral vascular accident, coma greater than 24 h, cardiac arrest, myocardial infarction, need for transfusion greater than four units postoperatively, sepsis, septic shock, and return to the operating room. All clinical factors in the ACSNSQIP database are defined in the user guide.14 Patients were grouped into octogenarians (80 y) and nonoctogenarians (<80 y). Categorical variables were analyzed between the two groups by chi-square test and continuous variables with Student’s t-test and ManneWhitney U test where appropriate. In addition, multivariate stepwise logistic regression was used to evaluate advanced age as an independent variable on occurrence of mortality and major postoperative complications. We also studied other clinically relevant preoperative variables to
generate odds ratios for factors associated with mortality and occurrence of major complications. All statistical analyses were performed on SPSS for Windows version 23 (SPSS Inc, Chicago, IL).
Results Patient demographics and characteristics We identified 2591 gastrectomies performed for malignancy in the NSQIP database. The average age of the cohort was 66.6 13.7 y. Of these patients, 487 were octogenarians (mean age, 83.8 3.1 y). A significantly higher proportion of octogenarians had cardiac, pulmonary, and neurologic comorbidities compared to nonoctogenarians. Furthermore, a higher proportion of octogenarians had American Society of Anesthesiology III/IV classifications, worse functional status, and lower average body mass index compared to nonoctogenarians. Overall, 4.9% of the patients who underwent gastrectomy had a diagnosis of disseminated cancer. However, the proportion of patients with disseminated cancer, the sex profile, and preoperative weight loss were similar between the two groups (Table 1).
Treatment characteristics A significantly lower proportion of octogenarians underwent radiation therapy (0.8% versus 3.2%, P ¼ 0.004) and chemotherapy (1.6% versus 7.3%, P < 0.001) before gastrectomy compared to nonoctogenarians. However, the rate of a prior surgery within 30-d before gastrectomy was similar between the two groups (0.8% versus 1.4%, P ¼ 0.360). Octogenarians underwent less extensive operations compared to nonoctogenarians. Only 24.0% of octogenarians underwent total gastrectomy compared to 43.2% of nonoctogenarians (P < 0.001). In addition, fewer octogenarians underwent extended lymphadenectomy (10.1% versus 17.4%, P < 0.001). The rates of additional organ resection were similar between the two groups except for pancreatic resection, which was greater in the nonoctogenarian group (2.8% versus 1.6%, P < 0.042). Additional operative details are summarized in Table 2.
Outcomes The rate of 30-d mortality in this overall cohort was 3.4%, and the rate of major complications was 26.5%. The 30-d mortality rate in octogenarians was nearly 3 times that of nonoctogenarians (7.2% versus 2.5%, P < 0.001). In addition, octogenarians experienced significantly higher rates of major complications compared to nonoctogenarians (31.4% versus 25.5% P ¼ 0.008), even with less extensive operations. Specifically, in descending order, the rates of pulmonary complications, septic shock, and cardiac complications were significantly higher in octogenarians. The rates of pneumonia and unplanned intubation were almost twice as high in the octogenarian group. However, the average time to death and the length of stay were similar between the two groups (Table 3).
3
teng et al gastrectomy in octogenarians
Table 1 e Comparison of demographics and comorbidities between octogenarians and nonoctogenarians. Characteristics
Age (mean)
Female Disseminated cancer
0.752
1235 (58.7)
273 (56.1)
History of TIA
51 (2.4)
35 (7.2)
<0.001
868 (41.3)
214 (43.9)
53 (2.5)
18 (3.7)
0.152
105 (5.0)
22 (4.5)
History of CVA and/or neurologic deficit History of CVA and/or no neurologic deficit
34 (1.6)
20 (4.1)
0.001
0.499
0.663 <0.001
88 (18.1) 349 (71.7)
IV
106 (5.0)
49 (10.1)
4 (0.1)
Diabetes Chronic steroid use <0.001
2020 (96.0)
441 (90.6)
75 (3.6)
40 (8.2)
9 (0.4)
6 (1.2)
CNS comorbidities
Endocrine history
1 (0.2)
Functional status (before surgery)
Ascites
ETOH (2 drinks/d 2 wk before surgery)
2042 (97.1)
471 (96.7)
0.694
26.7 6.4
25.1 5.2
0.001
>10% Weight loss in last 6 mo
359 (17.1)
70 (14.4)
0.150
Do not resuscitate status (yes)
8 (0.4)
4 (0.8)
0.196
381 (18.1)
94 (19.3)
0.540
34 (1.6)
11 (2.3)
0.328
Gastrointestinal history
Smoker (within 1 y)
Transfer status
BMI (mean)
2 (0.4)
0.001
742 (35.3)
Admitted from home
11 (0.5)
83.8 3.1
1252 (59.5)
Totally dependent
Preoperative dialysis dependence
62.6 11.9
III
Partially dependent
P value
P value
I-II
Independent
Aged 80 y, (n ¼ 487), n (%)
Aged 80 y, (n ¼ 487), n (%)
ASA class
Unknown
Aged <80 y, (n ¼ 2104), n (%)
Aged <80 y, (n ¼ 2104), n (%)
Gender Male
Table 1 e (continued ) Characteristics
13 (0.6)
5 (1.0)
0.328
455 (21.6)
25 (5.1)
<0.001
72 (3.4)
11 (2.3)
0.189
ASA class ¼ American Society of Anesthesiology Classification System; BMI ¼ body mass index; CHF ¼ congestive heart failure; CNS ¼ central nervous system; COPD ¼ chronic obstructive pulmonary disease; CVA ¼ cerebral vascular accident; ETOH ¼ alcohol abuse; heme ¼ hematology; HTN ¼ hypertension; meds ¼ medications; MI ¼ myocardial infarction; onc ¼ oncology; PCI ¼ percutaneous coronary intervention; TIA ¼ transient ischemic attack.
Preoperative comorbidities Cancer history (heme/ onc) Radiotherapy (<90 d)
68 (3.2)
4 (0.8)
0.004
Prior chemotherapy (<30 d)
154 (7.3)
8 (1.6)
<0.001
83 (3.9)
28 (5.7)
0.076
Bleeding disorders Cardiovascular history HTN (requiring meds)
<0.001
1094 (52.0)
376 (77.2)
MI (within 6 mo)
13 (0.6)
4 (0.8)
0.616
CHF (within 30 d before surgery)
16 (0.8)
7 (1.4)
0.151
Angina (in 1 mo before surgery)
13 (0.6)
9 (1.8)
0.008
Cardiac surgery
118 (5.6)
62 (12.7)
<0.001
PCI
136 (6.5)
61 (12.5)
<0.001
35 (1.7)
15 (3.1)
250 (11.9)
82 (16.8)
No dyspnea
1854 (88.1)
405 (83.2)
Severe COPD
100 (4.8)
42 (8.6)
4 (0.2)
1 (0.2)
History of distal revascularization Pulmonary history Dyspnea at rest/exertion
0.041 0.003
Discussion
Renal history Preoperative acute renal failure
On multivariate analysis, age 80 y was an independent risk factor associated with death (OR, 3.0; 95% CI, 1.9-4.9; P ¼ 0.003). The strongest predictor of death was performance of concomitant small bowel resection (OR, 4.6; 95% CI, 2.0-10.7; P < 0.001) followed by splenectomy and colon resection. Additional factors associated with mortality include total gastrectomy, pre-operative weight loss, dyspnea, and functional dependence (Table 4). Extended lymphadenectomy was not associated with increased mortality (OR, 1.0, 95% CI, 0.81.3, P ¼ 0.797). Age 80 y was also an independent risk factor associated with the occurrence of major complications (OR, 1.3; 95% CI, 1.03-1.6; P ¼ 0.025) on multivariate analysis. Other factors associated with the occurrence of major complications include total gastrectomy, additional organ resection, preoperative dialysis, and functional dependence (Table 5). Extended lymphadenectomy was not associated with an increase in morbidity (OR, 0.97; 95% CI, 0.76-1.23; P ¼ 0.790).
0.945 (continued)
Despite the improvement in perioperative care and modern surgical technique, gastrectomies performed for malignancy in the United States carry high perioperative morbidity and mortality. Our analysis serves as the largest study to date of octogenarians undergoing gastrectomy. The octogenarian
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Table 2 e Treatment details.
Table 3 e Postoperative adverse events.
Characteristics
Aged < 80 y, (n ¼ 2104), n (%)
Aged 80 y, (n ¼ 487), n (%)
P value
Characteristics
Anesthesia time (min)
300.3 120.2
265.0 107.2
<0.001
Death
Surgery time (min)
237.1 104.0
201.0 90.2
0.003
Preoperative treatment Prior surgery (within 30 d)
29 (1.4)
4 (0.8)
0.360
Radiotherapy (<90 d)
68 (3.2)
4 (0.8)
0.004
Prior chemotherapy (<30 d)
154 (7.3)
8 (1.6)
<0.001
Total gastrectomy Partial gastrectomy
908 (43.2)
117 (24.0)
1196 (56.8)
370 (76.0)
<0.001
Extended lymphadenectomy
366 (17.4)
49 (10.1)
Pancreatic resection
39 (2.8)
20 (1.6)
Hepatic resection Splenectomy
28 (1.3)
4 (0.8)
<0.001 0.042 0.359
113 (5.4)
18 (3.7)
0.129
Esophagectomy
17 (0.8)
3 (0.6)
0.663
Small bowel resection
62 (2.9)
12 (2.5)
0.564
Colectomy
60 (2.9)
15 (3.1)
0.786
Intraoperative or postoperative transfusion (yes)
143 (6.8)
44 (9.0)
0.083
Return to operating room
173 (8.2)
29 (6.0)
0.093
P value
<0.001
53 (2.5)
35 (7.2)
12.5 8.2
12.8 7.6
0.867
Days to discharge
10.8 8.5
11.9 9.5
0.020
Return to operating room
173 (8.2)
29 (6.0)
0.093
Major complications
537 (25.5)
153 (31.4)
0.008
MI
19 (0.9)
10 (2.1)
0.030
Cardiac arrest
27 (1.3)
13 (2.7)
0.025
Cardiac complications
Pulmonary complications 121 (5.8)
53 (10.9)
<0.001
Unplanned intubation
97 (4.6)
45 (9.2)
<0.001
Ventilator dependence > 48 h
107 (5.1)
31 (6.4)
0.257
Pulmonary emboli
25 (1.2)
7 (1.4)
0.654
Deep venous thrombosis
29 (1.4)
7 (1.4)
0.994
Acute renal failure requiring dialysis
14 (0.7)
7 (1.4)
0.087
Progressive renal insufficiency
13 (0.6)
3 (0.6)
0.996
Cerebral vascular accident with deficit
8 (0.4)
4 (0.8)
0.196
Coma >24 h
6 (0.2)
2 (0.4)
0.338
158 (7.5)
29 (6.0)
0.232
82 (3.9)
35 (7.2)
0.002
Renal complications
Neurologic complications
Infectious complications Sepsis Septic shock
cohort underwent less extensive operations compared to nonoctogenarians as evidenced by a lower rate of total gastrectomy (24.0 versus 43.2%) and extended lymphadenectomy (10.1% versus 17.4%). Despite less extensive surgical procedures, octogenarians still experienced a higher rate of complications and mortality compared to nonoctogenarians. Our study is noteworthy in that extended lymphadenectomy was not an independent predictor of worse outcomes. In the Dutch gastric cancer trial, extended lymphadenectomy (D2) resulted in significantly higher postoperative mortality compared to the limited lymphadenectomy (D1) offsetting any potential long-term effect in survival.15 However, in the Dutch trial, splenectomy was routinely performed as part of the D2 dissection. In our study, extended lymphadenectomy without additional organ resection did not increase postoperative mortality or morbidity. This suggests that in the modern surgical era, extended lymphadenectomy can be safely performed. While the ACS-NSQIP database, does not explicitly define extended lymphadenectomy as D1, D2, or state the number of nodes harvested, it describes a regional lymphadenectomy which goes well beyond harvesting just the perigastric nodes (regional lymph node dissection including celiac, gastric, portal, peripancreatic with or without the para-aortic, and vena cava regions). Furthermore, octogenarians received
Aged 80 y, (n ¼ 487), n (%)
Days to death
Pneumonia
Additional procedures performed
Aged < 80 y, (n ¼ 2104), n (%)
Urinary tract infection Superficial wound infection Deep incisional wound infection Wound disruption Organ space infection
84 (4.0)
27 (5.5)
0.128
119 (5.7)
29 (6.0)
0.798
36 (1.7)
3 (0.6)
0.074
35 (1.7)
6 (1.2)
0.492
146 (6.9)
26 (5.3)
0.201
MI ¼ myocardial infarction.
significantly less preoperative chemotherapy and radiation therapy. Previous studies with smaller patient populations have shown increased morbidity and mortality for octogenarians undergoing gastrectomy.12,15 However, our study is the first to show in such a large cohort that age 80 y itself confers a significantly higher risk for 30-d perioperative complications and a three times higher 30-d mortality risk on multivariate analysis. These results suggest that surgeons need to place greater emphasis on preparing and optimizing the octogenarian population before heading to the operating room. In a recent study, however, Ghignone et al. surveyed 251 surgical members of either the European Society of Surgical Oncology or the Society of Surgical Oncology and found that the majority of surgeons do not consider age as a potential limitation to
teng et al gastrectomy in octogenarians
Table 4 e Multivariate analysis of preoperative factors associated with an occurrence of a major complication. Prognostic factors Age 80 y
Adjusted, OR (95% CI) 1.3 (1.03-1.6)
P value 0.025
Total gastrectomy
1.6 (1.3-1.9)
<0.001
Colon resection
2.7 (1.7-4.5)
<0.001
Pancreatic resection
2.3 (1.3-4.2)
0.004
Splenectomy
1.6 (1.1-2.3)
0.019
Preoperative dialysis
3.4 (1.04-11.3)
0.042
CI ¼ confidence interval; OR ¼ odds ratio.
surgery. They also found that only about one-third of those surgeons coordinate their patient’s care with a geriatrician.16 Another recent study by Sakurai et al.17 examined the preoperative nutritional status of 594 patients with gastric cancer that underwent gastrectomy and found that 5-y survival was significantly worse in the patient cohort with a lower preoperative nutritional status. Combined with the current literature, our results strongly suggest that further research into the optimization and the multidisciplinary coordination of preoperative care of the octogenarian population is necessary in an attempt to improve postoperative morbidity and mortality for gastrectomy. Our examination of the ACS-NSQIP database also shows that there may be room for improvement in patient selection in both patient cohorts. Approximately 5% of the patients in the ACS-NSQIP database who underwent elective gastrectomy for malignancy had disseminated cancer, with no difference between octogenarians and nonoctogenarians (4.5% versus 5.0%). The current National Cancer Comprehensive guideline states that carcinomas should be considered unresectable in the case of positive peritoneal cytology (M1 disease) even in the absence of gross peritoneal disease and that gastric resection should be reserved for palliation of symptoms (obstruction or uncontrollable bleeding).18 In a retrospective review of 1241 patients at the Memorial Sloan Kettering Cancer Center who underwent laparoscopy with peritoneal washing for gastric cancer, 291 (23%; 198 with visible metastatic disease and 93 without gross disease but positive
5
cytology) patients had metastatic disease.19 Therefore, it is possible that the use of diagnostic laparoscopy with peritoneal lavage as a separate staging procedure may have helped to avoid unnecessary gastrectomies in patients with disseminated cancer. Another limitation of this study is that we were unable to determine whether gastrectomy was performed open or laparoscopic. Currently, outside of high-volume centers, laparoscopic resection of gastric cancer is not commonly performed in the United States.17 However, groups with extensive experience from both the West (United States and Europe) and the East (Japan, Korea, and Taiwan) have shown that in carefully selected patients, a minimally invasive surgical approach can improve perioperative outcomes with equivalent oncologic outcomes.20-26 Other studies examining the benefits of minimally invasive surgery for elderly patients undergoing different anatomic resections have also been performed. For example, Frasson et al. performed a randomized study comparing the effects of open and laparoscopic colorectal resections in patients <70 and patients 70. They concluded that laparoscopy in this case improved short-term outcomes for the elderly cohort more so than in the younger population.27 Further study into the laparoscopic approach for gastrectomy in the octogenarian population is warranted.
Conclusions To our knowledge, this is the largest series of octogenarians undergoing gastrectomy for malignancy in the literature. Perioperative morbidity and mortality of gastrectomy performed for malignancy is high, especially for octogenarians, in the United States. However, extended lymphadenectomy without additional organ resection did not increase morbidity or mortality in either patient cohort. Given such a high rate of perioperative morbidity and mortality, preoperative nutritional optimization as well as coordination of care for octogenarians undergoing gastrectomy may be an avenue to decrease their postoperative complications. Further research into preoperative care for octogenarians is necessary. Also, careful patient selection is paramount to avoid the potential complications of gastrectomy in patients who will not benefit from the operation. In our study, we found that nearly 5% of patients had disseminated cancer. Careful staging of these patients may reduce unnecessary operations.
Table 5 e Multivariate analysis of preoperative factors associated with 30-d mortality. Prognostic factors Age 80 y
Adjusted, OR (95% CI) 3.0 (1.9-4.9)
P value 0.003
Total gastrectomy
2.0 (1.3-3.3)
0.003
Colonic resection
3.2 (1.4-7.7)
0.007
Small bowel resection
4.6 (2.0-10.7)
<0.001
Splenectomy
3.5 (1.8-6.8)
<0.001
Weight loss
1.8 (1.1-3.1)
0.018
Dyspnea
1.8 (1.04-3.1)
0.036
Functionally dependent
2.7 (1.4-5.3)
0.003
CI ¼ confidence interval; OR ¼ odds ratio.
Acknowledgment The American College of Surgeon’s National Surgical Quality Improvement Program and the hospitals participating in the ACS-NSQIP are the source of the data used herein: they have not verified and are not responsible for the statistical validity of the data analysis or the conclusions derived by the author. Authors’ contributions: Conception and design were done by D.Y.L., A.T., A.J.B., and F.A. Analysis and interpretation and drafting of the article were executed by D.Y.L., A.T., G.B., M.P., E.P., and K.R. Data collection was carried out by D.Y.L., A.T.,
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and E.P. Critical revision was done by A.J.B., K.R., F.A., G.B., D.Y.L., and A.T. 14.
Disclosure 15.
The authors report no proprietary or commercial interest in any product mentioned or concept discussed in this article. 16.
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