METHODS: From the Nationwide Inpatient Sample (NIS, 2003-2009), the National Surgical Quality Improvement Project (NSQIP, 2005-2010), and the Surveillance Epidemiology and End Results (SEER, 2003-2009) databases using appropriate diagnostic and procedural codes we identified all patients with a diagnosis of a benign or malignant lesion of the body and/or tail of the pancreas that had undergone a partial or distal pancreatectomy. Utilization of laparoscopy was defined in NIS by the International Classification of Diseases, Ninth Revision correspondent procedure code; and in NSQIP by the exploratory laparoscopy or unlisted procedure current procedural terminology codes. In SEER, patients were identified by the International Classification of Diseases for Oncology, Third Edition diagnosis codes and the SEER Program Code Manual, third edition procedure codes. We analyzed the databases with respect to trends of inpatient outcome metrics, oncologic outcomes, and hospital volumes in patients with lesions of the neck and body of the pancreas that underwent operative resection.

RESULTS: NIS, NSQIP and SEER identified 4242, 2681 and 11  082 DP resections, respectively. Overall, laparoscopy was utilized in 15% (NIS) and 27% (NSQIP). No significant increase was seen over the course of the study. Resection was performed for malignancy in 59% (NIS) and 66% (NSQIP). Neither patient Body mass index nor comorbidities were associated with operative approach (P = 0.95 and P = 0.96, respectively). Mortality (3% vs 2%, P = 0.05) and reoperation (4% vs 4%, P = 1.0) was not different between laparoscopy and open groups. Overall complications (10% vs 15%, P < 0.001), hospital costs [44  741 dollars, interquartile range (IQR) 28 347-74 114 dollars vs 49 792 dollars, IQR 13 299-73 463, P = 0.02] and hospital length of stay (7 d, IQR 4-11 d vs 7 d, IQR 6-10, P < 0.001) were less when laparoscopy was utilized. One and two year survival after resection for malignancy were unchanged over the course of the study (ductal adenocarinoma 1-year 63.6% and 2-year 35.1%, P = 0.53; intraductal papillary mucinous neoplasm and nueroendocrine 1-year 90% and 2-year 84%, P = 0.25). The majority of resections were performed in teaching hospitals (77% NIS and 85% NSQIP), but minimally invasive surgery (MIS) was not more likely to be used in teaching hospitals (15% vs 14%, P = 0.26). Hospitals in the top decile for volume were more likely to be teaching hospitals than lower volume deciles (88% vs 43%, P < 0.001), but were no more likely to utilize MIS at resection. Complication rate in teaching and the top decile hospitals was not significantly decreased when compared to non-teaching (15% vs 14%, P = 0.72) and lower volume hospitals (14% vs 15%, P = 0.99). No difference was seen in the median number of lymph nodes and lymph node ratio in N1 disease when compared by year (P = 0.17 and P = 0.96, respectively).

The use of laparoscopy in distal pancreatectomy was first described in a porcine model by Soper et al[⁴] in 1994. Soon after this reports of laparoscopy in human patients were reported[⁵], though for many years laparoscopy was used principally for staging of malignancy. Multiple reports have shown that laparoscopic pancreatic resection is safe and feasible for benign and malignant pancreas lesions[^6-9]. The known benefits of laparoscopic approach such as lower intraoperative blood loss, less pain and analgesic requirements, earlier return of bowel function, shorter recovery and hospital stay have also been shown in pancreas surgery, including high quality clinical trials[^9-13]. Importantly, it has been reported that complication rates are lower after laparoscopic resection[^9,14].

There has been recent interest in improving the oncologic aspects of distal pancreas resection with attention to margins and lymph node harvest, oncological surrogate markers for oncological resection. During open or laparoscopic distal pancreatectomy in patients with peripancreatic and retropancreatic invasion, negative surgical margins and appropriate lymph node harvest can be accomplished if wider and deeper dissection techniques are used[^15,16]. It is unclear if this attention to a more radical resection has affected the practice of oncological surgical resection. Strasberg et al[¹⁶] reported that after open radical antegrade modular pancreatosplenectomy procedure for patients with adenocarcionoma of the body and tail of the pancreas outside the capsule, a negative tangential margin was accomplished in 91% of the patients.

Recent reports have not shown any difference between open and laparoscopic operations in regards to these oncological surrogate markers[^{8,10,11,15,16}].

Due to the association of higher hospital procedure volumes and improved clinical outcomes in complex oncologic operations, there has been interest in centralizing pancreas resections to high-volume hospitals. Current reports have documented the trend towards centralization of pancreatic procedures in the last decade, and report an improvement in perioperative mortality when these procedures are performed in high-volume hospitals[^17-20]. It has not been determined whether this centralization has occurred with distal pancreas resection.

Patients’ demographic characteristics included age, gender and body mass index. The comorbidities considered in NIS were acquired immune deficiency, alcohol abuse, iron deficiency anemia, rheumatoid arthritis, collagen vascular diseases, chronic blood loss anemia, congestive heart failure, chronic pulmonary disease, coagulopathy, uncomplicated diabetes, diabetes with chronic complications, hypertension, liver disease, fluid and electrolyte disorders, obesity, peripheral vascular disorders, renal failure and cardiac valve disease. Postoperative complications of interest in NSQIP were superficial surgical site infection, deep incisional surgical site infection, organ space surgical site infection, pneumonia, unplanned intubation, pulmonary embolism, renal insufficiency, stroke with neurological deficit, coma, peripheral nerve injury, cardiac arrest requiring CPR, myocardial infarction, intraoperative or postoperative transfusions, deep vein thrombosis requiring therapy, sepsis and septic shock. The type of hospital (teaching or non-teaching) was assessed by a specific variable in the NIS database. We defined high volume hospitals as the top decile for volume (with ≥ 11 cases per year) over the course of this study (NIS).

Overall, we found that in patients where laparoscopy was utilized, the median length of stay was shorter. This reinforces the findings of single center studies[^8,12,15,24]. Recently, Venkat et al[⁹] in a meta-analysis reported that patients that underwent a laparoscopic distal pancreatectomy had not just a lower blood loss and hospital length of stay, but also had fewer complications and surgical site infections. Importantly, no difference was found in operative time, margin positivity, incidence of postoperative pancreatic fistula or mortality. Additionally, we found that utilization of laparoscopy reduced overall expenses; this finding is likely secondary to the shorter length of stay and lower complication rate.

Other recent reports have confirmed the advantages of laparoscopic distal pancreatectomy over open approach, in terms of lower intraoperative blood loss, pain and analgesic requirements, earlier return of bowel function, shorter recovery and hospital stay[^{9,10,14,25,26}]. Therefore, the subset of patients with medical comorbidities could potentially benefit more than healthier patients, but we did not find that patient morbidity was associated with use of minimally invasive surgery.

Despite the known and reported benefits, overall laparoscopy was utilized in 15% (NIS) and 27% (NSQIP) of the distal pancreas resection cases. This represents all patients that had laparoscopy performed for diagnosis, staging, resection or a combination of these procedures. The rate of utilization of laparoscopy has remained stable over most of the past decade, although we could not determine in each case the specific technique of laparoscopy used. The finding of no increase in utilization of laparoscopy could be explained by the low number of pancreas surgeons that perform laparoscopic pancreatic resection. Also, another potential explanation for this stable rate could be that more laparoscopic resections and fewer diagnostic staging procedures are being performed over the study course, but these changes could not be detected by our analysis.

In our analysis, we showed that laparoscopy was utilized more frequently in malignant lesions, which could be due to utilization of laparoscopy for diagnosis and/or staging purposes. Interestingly, we did not find that laparoscopy was utilized and performed more frequently in teaching or high volume hospitals, though we expected that teaching hospitals and specialized medical centers would perform more MIS resection cases. It is not surprising that NSQIP hospitals have a higher rate of laparoscopy utilization than NIS hospitals, because NSQIP hospitals have volunteered for the program in an effort to improve quality. But it would not be appropriate to further compare data across different databases.

No consensus exists for or against the use of laparoscopic approach for distal pancreatectomy in malignant lesions, though recent publications support this approach in selected patients[⁷]. It has also been reported that after laparoscopic distal pancreatectomy in patients with invasion, a resection to negative margins and adequate lymph node harvest can be accomplished[¹⁵]. We also found that postoperative complications were more common after resection of malignant lesions, but even in malignant lesions use of laparoscopy was associated with a decrease in complications. The reported laparoscopic distal pancreatectomy morbidity ranges from 20% to 47% and the reported mortality rate ranges from 3% to 5%[^14,27,28]. Our study shows that nationwide mortality is at or below the benchmark reported data. The most common reported complications after laparoscopic distal pancreatectomy are pancreatic fistula, intra-abdominal abscesses, wound infection, sepsis, malabsortion, electrolyte disturbance and hemorrhage[^14,27,28]. The rate of intra-abdominal infection we report (9%) is also at or below reported benchmarks. This may reflect inaccuracy of coding.

Regarding oncological outcomes, no increase was seen in the number of lymph nodes harvested and lymph node ratio in N1 disease. More importantly the 1-year and 2-year survival did not increase during the course of this study.

The oncological surrogate markers associated with survival in pancreas cancer such as tumor size, tumor differentiation, surgical margins, lymph node status and lymph node ratio have been well documented[^{8,10,11,15,29}]. We speculate that surgeons might opt for open operation to enable a more radical oncologic resection. This however, does not appear to be the case, as survival and oncologic surrogate markers were unchanged over the course of the study. We believe that published data support using MIS to perform a more radical oncologic resection, but these data show this is not a common practice across the country[^8,15,16,30].

Multiple reports support centralization of oncological pancreas procedures towards high-volume hospitals, and as a result of this, a decrease in mortality has also been reported[^17-20]. Stitzenberg et al[¹⁸] analyzed the NIS database to assess cancer surgery centralization for pancreas, esophagus and colon cancer. Interestingly, during the course of the study there was a decrease in total number of hospitals performing pancreas procedures, but a statistical significant increase in the number of high-volume hospitals and a decrease in low-volume hospitals performing pancreatectomy procedures. All the high-volume centers were teaching hospitals. A total of 8.3% patients with a diagnosis of pancreas malignancy were admitted through an emergency room, and were more likely to have surgery done in a low-volume hospital.

Forces opposing the trend for centralization include the technological advances in imaging, resulting in diagnosis of pancreas lesions at earlier stages. Smaller lesions could potentially be managed in a non-specialized hospital, and only complicated cases referred to specialized hospitals. On the other hand, recent reports and guidelines support the use of endoscopic ultrasound with guided fine-needle aspiration for diagnosis and staging of body and tail pancreatic neoplasms[^31,32]. This procedure is usually performed in specialized medical centers, which would support the concept of centralization. In our analysis, centralization of distal pancreas procedures over the last decade has not occurred.

Even though the definition of utilization of laparoscopy in our analysis was broad, it appears that at a nationwide level, laparoscopy is underutilized for distal pancreas resection despite sufficient evidence of its benefit. Centralization of distal pancreas resections to high volume centers does not appear to be occurring in the United States, but this does not appear to affect overall quality. During the course of this study survival and extent of lymph node harvest has not changed.