- Email: [email protected]
Preoperative endoscopic tattooing of pancreatic body and tail lesions decreases operative time for laparoscopic distal pancreatectomy
Preoperative endoscopic tattooing of pancreatic body and tail lesions decreases operative time for laparoscopic distal pancreatectomy Naeem A. Newman, MD,a Anne Marie Lennon, MD, PhD,b Barish H. Edil, MD,a Marta M. Gilson, PhD,a Samuel A. Giday, MD,b Marcia I. Canto, MD,b Richard D. Schulick, MD, MHS,a and Martin A. Makary, MD, MPH,a Baltimore, MD
Background. Precise and expedient localization of small pancreatic tumors during laparoscopic distal pancreatectomy can be difficult owing to the decreased tactile ability of laparoscopy and the homogenous appearance of the surrounding retroperitoneal fat. Precise localization of the lesion is critical to achieving adequate margins of resection while preserving as much healthy pancreas as possible. The objective in this study was to determine the effect of endoscopic tattooing of the distal pancreas on operative time. Methods. We reviewed retrospectively 36 consecutive patients who had a laparoscopic distal pancreatectomy at our institution over a 4-year period (2006--2009). Ten patients underwent preoperative tattooing via an endoscopic transgastric technique using ultrasound guidance. The tattoo was performed using 2--4 cc of sterile purified carbon particles injected immediately proximal and anterior to the pancreatic lesion. Operative times were compared according to the presence of a tattoo. Results. The endoscopically placed tattoo was easily visible upon entering the lesser sac in all 10 patients at laparoscopy. Patients with a tattoo had a shorter operative time (median, 128.5 minutes; range, 53--180) compared with patients without a tattoo (median, 180 minutes; range, 120--240; P < .01). None of the tattoo group required repeat surgery, whereas 1 patient who was not tattooed required re-resection for a lesion missed in the initial specimen. There were no complications associated with the endoscopic ultrasound-guided tattoo. Conclusion. Endoscopic ultrasound-guided tattooing of pancreas lesions before a laparoscopic distal pancreatectomy is safe and is associated with decreased operative time compared with nontattooed patients. This technique can allow for quick and precise localization of the lesion, allowing for optimal preservation of pancreas parenchyma and demarcating an appropriate line of resection. (Surgery 2010;148:371-7.) From the Departments of Surgerya and Gastroenterology,b The Johns Hopkins Hospital, The Johns Hopkins University School of Medicine, Baltimore, MD
LAPAROSCOPIC DISTAL PANCREATECTOMY can spare a patient the risks and morbidity associated with an open operation.1-8 However, lesions of the body and tail can be difficult to localize at the time of laparoscopy because they can be small, intraparenchymal lesions, and posterior. Precise localization N.A.N. and A.M.L. contributed equally to this manuscript. Supported by a grant from The Chad and Nissa Richison Family Foundation. Accepted for publication April 13, 2010. Reprint requests: Martin A. Makary, MD, MPH, Department of Surgery, Johns Hopkins Hospital, CRB II, Suite 507, 1550 Orleans Street, Baltimore, MD 21231. E-mail: [email protected]. 0039-6060/$ - see front matter Ó 2010 Mosby, Inc. All rights reserved. doi:10.1016/j.surg.2010.04.008
of a lesion is critical to achieving adequate surgical margins while avoiding the unnecessary resection of healthy pancreatic tissue. Even large tumors, on preoperative imaging, which a surgeon can anticipate to be easy to identify, can be surprisingly difficult to find laparoscopically, given the decreased tactile sensation and the homogeneousappearing surrounding retroperitoneal fat.9 Endoscopic ultrasound (EUS)-guided tattooing of a pancreatic lesion has been described in single case reports using a tattoo.10-13 EUS-guided tattooing of distal pancreatic lesions was performed and operative outcomes were compared with patients who underwent conventional laparoscopic distal pancreatectomy. We hypothesized that the presence of a tattoo would allow rapid identification SURGERY 371
372 Newman et al
Surgery August 2010
of pancreatic lesions allowing for a precise resection of the tumor. METHODS Patients. A retrospective review was performed of 36 consecutive patients who underwent laparoscopic distal pancreatectomy at Johns Hopkins University Hospital from 2006 to 2009. The clinical records, EUS report, operative notes, and pathology reports were reviewed for each patient. The lesions were identified preoperatively by computed tomography. We did not ask for a biopsy for lesions which met surgical criteria radiographically. Visibility of the tattoo was assessed at the time of laparoscopy in patients who had undergone EUS-guided tattoo injection (Fig 1). Operative times, estimated blood loss, surgical margins, length of hospital stay, morbidity, and mortality were documented. Postoperative morbidity, defined as any complication arising in the 30-day postoperative period, was also recorded. Benign versus malignant pathologic diagnoses were made postoperatively. Endoscopic tattooing. EUS was routinely performed by 2 endosonographers before surgery. Endoscopy was performed using an Olympus UCT 140 linear echoscope (Olympus America Inc., Center Valley, PA). Once the lesion was identified, a 22-gauge EUS--fine needle aspiration needle (EchoTip Ultra; Wilson-Cook Medical, Winston-Salem, NC) was inserted 3--5 mm proximal to the lesion and 2--4 mL of sterile purified carbon particles (GI Spot; GI Supply, Camp Hill, PA) was injected under direct EUS visualization. Injection continued as the needle was withdrawn leaving an inked tract, with care taken to avoid peritoneal injection. Preprocedural antibiotics were given and continued for 3 days. Antibiotics were given after tattooing; however, we recognize that there are no data to support this practice and it has now been revisited. Laparoscopic distal pancreatectomy with and without spleen preservation. We begin by placing an umbilical port using a direct Hassan cut-down technique. Under direct visualization, we then insert 2 ports in the upper mid-line (or right of mid-line for more medial tumors) and 1 in the left lower quadrant. The precise location for these ports depends on the location of the tumor, the possibility of removing the spleen, and the patient’s body habitus. Once local landmarks are identified, the gastrocolic omentum and short gastric vessels are divided, followed by take-down of the splenic flexure of the colon to achieve wide visualization of the lesser sac. We stop the dissection once exposure is adequate and the tumor or tattoo is easily visible.
Fig 1. Illustration of the tattooing technique.
Once the tumor or tattoo is visualized, we mobilize the gland from its inferior border (Fig 2). The inferior approach facilitates dissection of the posterior aspect of the gland from the retroperitoneal bed. The splenic artery and vein branches can be visualized from underneath the pancreas, and we alternate dissection of the splenic vessels from above and below the gland because this exposure offers the best visualization. When splenic preservation is performed, the small branches of the splenic vessels to the pancreas parenchyma are individually dissected and divided; but when we include a splenectomy, we divide the splenic vessels individually with a gastrointestinal anastomosis stapler 2.5 mm (white vascular load) stapler. The gland is divided with an endogastrointestinal anastomosis stapler 2.5 or 3.5 mm (white vascular load or blue GI load) depending on pancreas thickness. The reticulating stapler is reinforced with a bioabsorbable staple line material. In patients with a pancreas tattoo, the pancreas is divided just proximal to the tattoo with a margin of $1 cm (Fig 3). Clear margins are confirmed on frozen section before closing. When there is a suspicion of malignancy or a technical reason necessitates removal of the spleen, we choose to mobilize the spleen after individual division of the splenic artery, vein, and gland. Statistical analysis. Fisher exact test was used to compare categorical variables, and the Wilcoxon rank-sum test was used to compare continuous variables because most variable did not appear to be normally distributed. Statistical analyses were performed with the use of SAS software, version 9.1 (SAS Institute Inc., Cary, NC). Results were considered significant if P < .05. RESULTS An endoscopically placed tattoo was performed preoperatively in 10 patients. The median time from tattooing to operative resection was 38 days (range,
Newman et al 373
Surgery Volume 148, Number 2
Fig 2. EUS FNA tattoo (white arrow) at laparoscopy.
1--83) before surgery. Tattooed and nontattooed patients were of a similar age and gender (Table I). Five of the tattooed resections were in the initial half of our experience with the procedure and the remaining 5 were in the latter half of our experience. Operative time was decreased in patients who had a preoperative tattoo because the tattoo was very useful in rapidly localizing the tumor and planning the line of resection (Table II). Median operative time was statistically significantly shorter in the tattoo group (128.5 vs 180 minutes in the nontattoo group; P = .01). All 10 tattoos were easily visible laparoscopically (Fig 1), including the tattoo placed 84 days before surgery. The median estimated blood loss was greater in the nontattoo group, although this was not significant using the Fisher exact test. (62.5 vs 10 mL in the tattooed group; P = .68). Two patients in the nontattoo group underwent a second operative procedure. The first required extension of the pancreatectomy, because no lesion was identified in the initial resection specimen and the second had postoperative bleeding that required reoperation. Postoperative morbidity, defined as any complication arising in the 30-day postoperative period, was 23% in the nontattoo group (n = 6) and 20% in the tattoo group (n = 2). There was 1 death in the nontattoo group (4%) owing to a postoperative arrhythmia that resulted in cardiac arrest. An extensive investigation revealed no evidence of anemia or cause related to the operative technique. Patients who had a laparoscopic resection with a tattoo had a decreased length of stay compared with nontattooed patients 4 days (range, 3--8) versus 5 days (range, 2--17), although this difference was not significant (P = .10). Major comorbidities were similar in both groups with a mean number of 1.1 major comorbidities in the tattoo group and 0.9 in the nontattoo group (P = .27). Histologic findings are shown in Table III. The most common indication for resection was a
neuroendocrine tumor, accounting for 50% (n = 5) of the tattoo cases and 31% (n = 8) of the nontattoo group. Adenocarcinoma accounted for 20% (n = 2) of the tattoo cases and 8% (n = 2) of the nontattoo group. Other lesions which were resected included serous cystadenoma, mucinous cystadenoma, intraductal papillary mucinous neoplasm and pancreatic pseudocyst. The median size of the tumor in the tattoo group was 0.7 cm smaller than in the nontattooed tumors (1.3 vs 2 cm; P = .04). One patient who was tattooed 12 hours before laparoscopy did demonstrate some mild pancreatitis. After this observation, we increased the time between tattooing and surgery to allow any such subclinical inflammation to resolve before operation. There were no other documented cases of acute pancreatitis in the patients who underwent EUS-guided tattoo placement on histology. DISCUSSION Laparoscopic distal pancreatectomy is increasingly being performed for tumors of the body and tail of the pancreas. Laparoscopic distal pancreatectomy was initially described by Gagner et al14 in 1996 for resection of pancreatic neuroendocrine tumors. Since then, there have been an increasing number of reports of laparoscopic distal pancreatectomy for a range of indications.9,15,16-39 Retrospective, case-control studies comparing laparoscopic distal pancreatectomy and open distal pancreatectomy have demonstrated significantly shorter hospitalization time for the laparoscopic group, with no significant difference in either operative time or rate of complications.1,13,17,40 Rationale of demarcation. One of the challenges faced by surgeons performing laparoscopic distal pancreatectomy is that lesions can be difficult to identify. Even lesions that are clearly visible
374 Newman et al
Surgery August 2010
Table I. Patient characteristics
Age at surgery, y (median, range) Male Female Time between EUS and LDP, days (median, range)
Tattoo group (n = 10)
Nontattoo group (n = 26)
60.5 (38–81)
61.5 (28–84)
4 (40%) 6 (60%) 38 (1–83)
12 (46%) 14 (54%) NA
EUS, Endoscopic ultrasound; LDP, laparoscopic distal pancreatectomy; NA, not applicable.
Fig 3. Resected specimen showing tattoo (white block arrow) proximal to the tumor (black thin arrow).
on imaging techniques may not be visible during laparoscopy as the lesion is deep in the parenchyma requiring palpation to localize.26 The challenge to appropriately localize small pancreatic tumors is not new to the era of laparoscopy. For example, small islet cell tumors of the pancreatic tail can be notoriously difficult to find using an open operative approach. Ultrasonography has been used in the past to locate pancreatic lesions intraoperatively and this technique has been used laparoscopically. We prefer tattooing pancreatic lesions over laparoscopic ultrasonography for many reasons. First, tattooing provides a more definitive localization in demarcating a line of resection. Studies have shown that intraoperative ultrasound has a sensitivity of 80--100%, although these studies use both palpation and ultrasound combined during open surgery. When ultrasound is performed laparoscopically, palpation is unavailable and the sensitivity of ultrasound is decreased.16,41-43 When attempted laparoscopically, an inability to localize with intraoperative ultrasonography can lead to conversion to open operation unnecessarily. In addition, laparoscopic ultrasound probes frequently do not provide the resolution of the standard intraoperative probes.2,16 Intraoperative ultrasound, either open or laparoscopic, may locate a tumor; however, it may not allow for precise marking in real time. Assessment of an intra-abdominal organ must be done in 2 separate planes to confirm a mass is really present. Also, visualization of the tattoo intraoperatively allows for directed dissection, limiting unnecessary exploration for the tumor and decreasing the risk of injury of surrounding structures. Tattooing also helps to ensure an adequate oncologic margin because the tattoo is
placed proximal to the lesion. Finally, we believe the precise localization offered by tattooing allows us to optimize the preservation of healthy pancreas parenchyma, mitigating the risk of future diabetes caused by unnecessary over-resection. Endoscopic tattooing of the pancreas was first described by Gress et al in 2002,11 who used India ink to identify an insulinoma before operative resection. After reports of complications associated with India ink, alternative methods of tattooing have been sought.44,45 There have been case reports of using indocyanine green ink,12 methylene blue,13 and GI spot10 to tattoo the pancreas, with no complications reported. EUS-guided fine needle aspiration is safe with a complication rate of 0--2.2%.46-49 Tumor seeding along the needle path is a potential complication of EUS-guided fine needle aspiration, however, it is very rare,50-52 with only 1 report of tumor seeding of a pancreatic adenocarcinoma.50 The risk of seeding with EUS-guided tattooing should be negligible, because the needle is placed proximal to, rather than within, the tumor. Another potential complication of endoscopic fine needle aspiration of the pancreas is pancreatitis with an incidence of 0--2% in the literature.46-49,53-55 There was no evidence of pancreatitis on histologic examination in our series. Endoscopic tattooing was performed a median of 38 days before laparoscopic distal pancreatectomy, with a range of up to 83 days. In all cases, the tattoo was clearly visible at laparoscopy (Fig 1). The importance of being able to identify the lesion is seen in this study where the lesion was identified and resected in all 10 tattooed patients. This contrasts with the nontattoo group, where 1 patient required a repeat operative procedure because an 8-mm insulinoma could not be visualized during laparoscopy. Intraoperative ultrasonography was performed during the first operative procedure and a small lesion identified in the tail of the
Newman et al 375
Surgery Volume 148, Number 2 Table II. Operative and postoperative details Tattoo group (n = 10) Operative procedure LDP Spleen-preserving LDP OR time, min (median, range) Estimated blood loss, mL (median, range) Conversion to open Complication rate Wound infection Pancreatic leak Abscess Postoperative bleeding Postoperative morbidity Time to discharge, days (median, range) Mortality
6 4 128.5 10
(60%) (40%) (53–180) (10–200)
Nontattoo group (n = 26) 17 9 180* 62.5
(65%) (35%) (120--240) (10–800)
0 (0%)
6 (23%)
0 2 0 0 2 4 0
1 4 0 1 6 5 1
(0%) (20%) (0%) (0%) (20%) (3–8) (0%)
(4%) (15.4%) (0%) (4%) (23%) (2–17) (4.5%)
Postoperative morbidity was defined as any complication arising in the 30-day postoperative period. *P < .05. NA, Not applicable.
Table III. Pathologic diagnosis in surgical resection specimen Tattoo group (n = 10)
Nontattoo group (n = 26)
Neuroendocrine 5 (50%) Adenocarcinoma 2 (20%) Serous cystadenoma 1 (10%) Mucinous cystadenoma 2 (20%) Chronic pancreatitis 0 IPMN 0 Pseudopapillary tumor 0 Size, cm (median, range) 1.3 (0.8–2.8) Node positive, n (%) 1 (12%)
8 (31%) 2 (8%) 5(19%) 3 (12%) 2 (8%) 4 (15%) 2 (8%) 2.0 (0.6–6.5) 2 (10%)
IPMN, Intraductal papillary mucinous neoplasm.
pancreas was resected. However, when the patient became hypoglycemic on postoperative day 3, it became apparent that this was a multifocal lesion and the preoperatively identified (by EUS) symptomatic lesion had not been resected. The patient then underwent endoscopic tattooing of the lesion, which was clearly visible on repeat laparoscopy and the lesion fully resected. Zografos et al13 reported a similar situation where a patient with a confirmed insulinoma found on EUS underwent laparotomy, but the lesion could not be identified despite the use of intraoperative ultrasound. Operative time. The median operative time was significantly greater in the nontattoo group 180 minutes (range, 120--240) versus 128.5 minutes (range, 53--180) in the tattoo group. This difference in operative times was significant (P = .01).
The results in both the nontattoo and tattoo groups are better than the literature, where the mean operative time is 220 minutes (range, 65-500).56 We believe the shorter operative time in the tattoo group is due to the ease with which the lesion was identified after tattooing. Unlike intraoperative ultrasonography, where lesions cannot be identified in 10--40% of cases,14,16,23,26,41 the lesion was identified in all 10 cases (100%) in this series. Median intraoperative blood loss was less in the tattoo group (10 vs 62.5 mL in the nontattoo group), although this was not significant (P = .68). This trend may have occurred because the tattoo spares unnecessary dissection. Postoperative morbidity and time to discharge were not different between the 2 groups. Preventing diabetes. Preservation of pancreatic parenchyma is an important goal of pancreas surgery. After distal pancreatectomy, 8--23% of patients develop new-onset diabetes.42,57 In addition, 61% will develop exocrine insufficiency after resection.42 Endoscopic tattooing allows the surgeon to precisely locate a lesion to within 3--5 mm, and could potentially limit the amount of pancreatic tissue resected. It is not possible to assess whether this is sufficient to affect the development of endocrine or exocrine pancreatic insufficiency in this retrospective study; larger, prospective studies are needed to examine this. Limitations. This study has several important limitations. It is a retrospective, single-center study based on the experience of 2 surgeons. There is a natural referral bias because patients who were
376 Newman et al
referred for EUS-guided tattooing had smaller tumors. In addition, it is difficult to control the many confounding variables that contribute to long operative times. Further studies are required to confirm the findings in this study. In conclusion, despite these limitations, the finding of decreased operative time is significant. We recommend endoscopic tattooing for patients undergoing laparoscopic distal pancreatectomy for tumors <4 cm. In our experience, tattooing decreases operative time and, more important, demarcates a precise line of resection to avoid the unnecessary resection of additional pancreatic parenchyma. We also believe that these findings are transferable to open operations in decreasing operative times by facilitating identification of small lesions. The authors thank Corrine Sandone for the artistic contributions to the manuscript and Mr and Mrs Chad and Nissa Richison for sponsoring this research. REFERENCES 1. Kooby D, Gillespie T, Nakeeb A, Hawkins W, et al. Left-sided pancreatectomy: a multicenter comparison of laparoscopic and open approaches. Ann Surg 2008;248:438-46. 2. Pryor A, Means JR, Pappas TN. Laparoscopic distal pancreatectomy with splenic preservation. Surg Endosc 2007;21: 2326-30. 3. Tang CN, Tsui KK, Ha JP, et al. Laparoscopic distal pancreatectomy: a comparative study. Hepatogastroenterology 2007;54:265-71. 4. Pierce RA, Spitler JA, Hawkins WG, et al. Outcomes analysis of laparoscopic resection of pancreatic neoplasms. Surg Endosc 2007;21:579-86. 5. Palanivelu C, Shetty R, Jani K, et al. Laparoscopic distal pancreatectomy: results of a prospective non-randomized study from a tertiary center. Surg Endosc 2007;21:373-7. 6. Baker MS, Bentrem DJ, Talamonti MS, et al. A prospective single institution comparison of peri-operative outcomes for laparoscopic and open distal pancreatectomy. Surgery 2009;146:635-45. 7. Finan KR, Cannon EE, Christein JD, et al. Laparoscopic and open distal pancreatectomy: a comparison of outcomes. Am Surg 2009;75:671-80. 8. Borja-Cacho D, Al-Refaie WB, Jensen EH, et al. Laparoscopic distal pancreatectomy. J Am Coll Surg 2009;209:758-65. 9. Jossart GH, Gagner M. Pancreaticoduodenal resection. J Hepatobiliary Pancreat Surg 2000;7:21-7. 10. Farrell JJ, Sherrod A, Parekh D. EUS-guided fine-needle tattooing for preoperative localization of early pancreatic adenocarcinoma. Gastrointest Endosc 2009;69:176-7. 11. Gress FG, Barawi M, Kim D, et al. Preoperative localization of a neuroendocrine tumor of the pancreas with EUS-guided fine needle tattooing. Gastrointest Endosc 2002;55:594-7. 12. Ashida R, Yamao K, Okubo K, et al. Indocyanine green is an ideal dye for endoscopic ultrasound-guided fine-needle tattooing of pancreatic tumors. Endoscopy 2006;38:190-2. 13. Zografos GN, Stathopoulou A, Mitropapas G, et al. Preoperative imaging and localization of small sized insulinoma with EUS-guided fine needle tattooing: a case report. Hormones (Athens) 2005;4:111-6.
Surgery August 2010
14. Gagner M, Pomp A, Herrera MF. Early experience with laparoscopic resections of islet cell tumors. Surgery 1996;120: 1051-4. 15. Cuschieri A, Jakimowicz JJ, van Spreeuwel J. Laparoscopic distal 70% pancreatectomy and splenectomy for chronic pancreatitis. Ann Surg 1996;223:280-5. 16. Jaroszewski DE, Schlinkert RT, Thompson GB, et al. Laparoscopic localization and resection of insulinomas. Arch Surg 2004;139:270-4. 17. Cuschieri SA, Jakimowicz JJ. Laparoscopic pancreatic resections. Semin Laparosc Surg 1998;5:168-79. 18. Patterson EJ, Gagner M, Salky B, et al. Laparoscopic pancreatic resection: single-institution experience of 19 patients. J Am Coll Surg 2001;193:281-7. 19. Fernandez-Cruz L, Herrera M, Saenz A, et al. Laparoscopic pancreatic surgery in patients with neuroendocrine tumours: indications and limits. Best Pract Res Clin Endocrinol Metab 2001;15:161-75. 20. Park AE, Heniford BT. Therapeutic laparoscopy of the pancreas. Ann Surg 2002;236:149-58. 21. Uranues S, Alimoglu O, Todoric B, et al. Laparoscopic resection of the pancreatic tail with splenic preservation. Am J Surg 2006;192:257-61. 22. Mabrut JY, Boulez J, Peix JL, et al. Laparoscopic pancreatic resection: a preliminary experience of 15 patients. Hepatogastroenterology 2005;52:230-2. 23. Mabrut JY, Fernandez-Cruz L, Azagra JS, et al. Laparoscopic pancreatic resection: results of a multicenter European study of 127 patients. Surgery 2005;137:597-605. 24. Misawa T, Shiba H, Usuba T, et al. Systemic inflammatory response syndrome after hand-assisted laparoscopic distal pancreatectomy. Surg Endosc 2007;21:1446-9. 25. Gramatica L Jr, Herrera MF, Mercado-Luna A, et al. Videolaparoscopic resection of insulinomas: experience in two institutions. World J Surg 2002;26:1297-300. 26. Ayav A, Bresler L, Brunaud L, et al. Laparoscopic approach for solitary insulinoma: a multicentre study. Langenbecks Arch Surg 2005;390:134-40. 27. Edwin B, Mala T, Mathisen O, et al. Laparoscopic resection of the pancreas: a feasibility study of the short-term outcome. Surg Endosc 2004;18:407-11. 28. D’Angelica M, Are C, Jarnagin W, et al. Initial experience with hand-assisted laparoscopic distal pancreatectomy. Surg Endosc 2006;20:142-8. 29. Dulucq JL, Wintringer P, Stabilini C, et al. Are major laparoscopic pancreatic resections worthwhile? A prospective study of 32 patients in a single institution. Surg Endosc 2005;19:1028-34. 30. Fernandez-Cruz L, Cosa R, Blanco L, et al. Curative laparoscopic resection for pancreatic neoplasms: a critical analysis from a single institution. J Gastrointest Surg 2007;11:1607-21. 31. Melotti G, Butturini G, Piccoli M, et al. Laparoscopic distal pancreatectomy: results on a consecutive series of 58 patients. Ann Surg 2007;246:77-82. 32. Han HS, Min SK, Lee HK, et al. Laparoscopic distal pancreatectomy with preservation of the spleen and splenic vessels for benign pancreas neoplasm. Surg Endosc 2005;19:1367-9. 33. Corcione F, Marzano E, Cuccurullo D, et al. Distal pancreas surgery: outcome for 19 cases managed with a laparoscopic approach. Surg Endosc 2006;20:1729-32. 34. Fernandez-Cruz L, Saenz A, Astudillo E, et al. Laparoscopic pancreatic surgery in patients with chronic pancreatitis. Surg Endosc 2002;16:996-1003. 35. Fabre JM, Dulucq JL, Vacher C, et al. Is laparoscopic left pancreatic resection justified? Surg Endosc 2002;16:1358-61.
Surgery Volume 148, Number 2
36. Vezakis A, Davides D, Larvin M, et al. Laparoscopic surgery combined with preservation of the spleen for distal pancreatic tumors. Surg Endosc 1999;13:26-9. 37. Van Nieuwenhove Y, Vandaele S, Op de Beeck B, et al. Neuroendocrine tumors of the pancreas. Surg Endosc 2003;17: 1658-62. 38. Berends FJ, Cuesta MA, Kazemier G, et al. Laparoscopic detection and resection of insulinomas. Surgery 2000;128: 386-91. 39. Briggs CD, Mann CD, Irving GR, et al. Systematic review of minimally invasive pancreatic resection. J Gastrointest Surg 2009;13:1129-37. 40. Larsen MH, Fristrup CW, Mortensen MB. Endoscopic ultrasound-guided fine-needle marking of a small pancreatic tumor. Endoscopy 2009;41(Suppl 2):E175-6. 41. Rosch T, Lightdale CJ, Botet JF, et al. Localization of pancreatic endocrine tumors by endoscopic ultrasonography. N Engl J Med 1992;326:1721-6. 42. Spitz JD, Lilly MC, Tetik C, Arregui ME. Ultrasound-guided laparoscopic resection of pancreatic islet cell tumors. Surg Laparosc Endosc Percutan Tech 2000;10:168-73. 43. Iihara M, Kanbe M, Okamoto T, Ito Y, Obara T. Laparoscopic ultrasonography for resection of insulinomas. Surgery 2001;130:1086-91. 44. Al-Haddad M, Wallace MB, Woodward TA, et al. The safety of fine-needle aspiration guided by endoscopic ultrasound: a prospective study. Endoscopy 2008;40:204-8. 45. Siddiqui UD, Rossi F, Rosenthal LS, et al. EUS-guided FNA of solid pancreatic masses: a prospective, randomized trial comparing 22-gauge and 25-gauge needles. Gastrointest Endosc 2009;70:1093-7. 46. Hikichi T, Irisawa A, Bhutani MS, et al. Endoscopic ultrasound-guided fine-needle aspiration of solid pancreatic masses with rapid on-site cytological evaluation by endosonographers without attendance of cytopathologists. J Gastroenterol 2009;44:322-8.
Newman et al 377
47. Fisher L, Segarajasingam DS, Stewart C, et al. Endoscopic ultrasound guided fine needle aspiration of solid pancreatic lesions: performance and outcomes. J Gastroenterol Hepatol 2009;24:90-6. 48. Paquin SC, Gariepy G, Lepanto L, et al. A first report of tumor seeding because of EUS-guided FNA of a pancreatic adenocarcinoma. Gastrointest Endosc 2005;61:610-1. 49. Doi S, Yasuda I, Iwashita T, et al. Needle tract implantation on the esophageal wall after EUS-guided FNA of metastatic mediastinal lymphadenopathy. Gastrointest Endosc 2008; 67:988-90. 50. Shah JN, Fraker D, Guerry D, et al. Melanoma seeding of an EUS-guided fine needle track. Gastrointest Endosc 2004;59: 923-4. 51. Iglesias-Garcia J, Dominguez-Munoz E, Lozano-Leon A, et al. Impact of endoscopic ultrasound-guided fine needle biopsy for diagnosis of pancreatic masses. World J Gastroenterol 2007;13:289-93. 52. Eloubeidi MA, Tamhane A. EUS-guided FNA of solid pancreatic masses: a learning curve with 300 consecutive procedures. Gastrointest Endosc 2005;61:700-8. 53. Yusuf TE, Ho S, Pavey DA, et al. Retrospective analysis of the utility of endoscopic ultrasound-guided fine-needle aspiration (EUS-FNA) in pancreatic masses, using a 22-gauge or 25-gauge needle system: a multicenter experience. Endoscopy 2009;41:445-8. 54. Fernandez-Cruz L, Saenz A, Astudillo E, et al. Outcome of laparoscopic pancreatic surgery: endocrine and nonendocrine tumors. World J Surg 2002;26:1057-65. 55. Gagner M, Pomp A. Laparoscopic pancreatic resection: Is it worthwhile? J Gastrointest Surg 1997;1:20-5. 56. Cho YB, Lee WY, Yun HR, et al. Tumor localization for laparoscopic colorectal surgery. World J Surg 2007;31:1491-5. 57. Lo CY, Lo CM, Fan ST. Role of laparoscopic ultrasonography in intraoperative localization of pancreatic insulinoma. Surg Endosc 2000;14:1131-5.
Background. Precise and expedient localization of small pancreatic tumors during laparoscopic distal pancreatectomy can be difficult owing to the decreased tactile ability of laparoscopy and the homogenous appearance of the surrounding retroperitoneal fat. Precise localization of the lesion is critical to achieving adequate margins of resection while preserving as much healthy pancreas as possible. The objective in this study was to determine the effect of endoscopic tattooing of the distal pancreas on operative time. Methods. We reviewed retrospectively 36 consecutive patients who had a laparoscopic distal pancreatectomy at our institution over a 4-year period (2006--2009). Ten patients underwent preoperative tattooing via an endoscopic transgastric technique using ultrasound guidance. The tattoo was performed using 2--4 cc of sterile purified carbon particles injected immediately proximal and anterior to the pancreatic lesion. Operative times were compared according to the presence of a tattoo. Results. The endoscopically placed tattoo was easily visible upon entering the lesser sac in all 10 patients at laparoscopy. Patients with a tattoo had a shorter operative time (median, 128.5 minutes; range, 53--180) compared with patients without a tattoo (median, 180 minutes; range, 120--240; P < .01). None of the tattoo group required repeat surgery, whereas 1 patient who was not tattooed required re-resection for a lesion missed in the initial specimen. There were no complications associated with the endoscopic ultrasound-guided tattoo. Conclusion. Endoscopic ultrasound-guided tattooing of pancreas lesions before a laparoscopic distal pancreatectomy is safe and is associated with decreased operative time compared with nontattooed patients. This technique can allow for quick and precise localization of the lesion, allowing for optimal preservation of pancreas parenchyma and demarcating an appropriate line of resection. (Surgery 2010;148:371-7.) From the Departments of Surgerya and Gastroenterology,b The Johns Hopkins Hospital, The Johns Hopkins University School of Medicine, Baltimore, MD
LAPAROSCOPIC DISTAL PANCREATECTOMY can spare a patient the risks and morbidity associated with an open operation.1-8 However, lesions of the body and tail can be difficult to localize at the time of laparoscopy because they can be small, intraparenchymal lesions, and posterior. Precise localization N.A.N. and A.M.L. contributed equally to this manuscript. Supported by a grant from The Chad and Nissa Richison Family Foundation. Accepted for publication April 13, 2010. Reprint requests: Martin A. Makary, MD, MPH, Department of Surgery, Johns Hopkins Hospital, CRB II, Suite 507, 1550 Orleans Street, Baltimore, MD 21231. E-mail: [email protected]. 0039-6060/$ - see front matter Ó 2010 Mosby, Inc. All rights reserved. doi:10.1016/j.surg.2010.04.008
of a lesion is critical to achieving adequate surgical margins while avoiding the unnecessary resection of healthy pancreatic tissue. Even large tumors, on preoperative imaging, which a surgeon can anticipate to be easy to identify, can be surprisingly difficult to find laparoscopically, given the decreased tactile sensation and the homogeneousappearing surrounding retroperitoneal fat.9 Endoscopic ultrasound (EUS)-guided tattooing of a pancreatic lesion has been described in single case reports using a tattoo.10-13 EUS-guided tattooing of distal pancreatic lesions was performed and operative outcomes were compared with patients who underwent conventional laparoscopic distal pancreatectomy. We hypothesized that the presence of a tattoo would allow rapid identification SURGERY 371
372 Newman et al
Surgery August 2010
of pancreatic lesions allowing for a precise resection of the tumor. METHODS Patients. A retrospective review was performed of 36 consecutive patients who underwent laparoscopic distal pancreatectomy at Johns Hopkins University Hospital from 2006 to 2009. The clinical records, EUS report, operative notes, and pathology reports were reviewed for each patient. The lesions were identified preoperatively by computed tomography. We did not ask for a biopsy for lesions which met surgical criteria radiographically. Visibility of the tattoo was assessed at the time of laparoscopy in patients who had undergone EUS-guided tattoo injection (Fig 1). Operative times, estimated blood loss, surgical margins, length of hospital stay, morbidity, and mortality were documented. Postoperative morbidity, defined as any complication arising in the 30-day postoperative period, was also recorded. Benign versus malignant pathologic diagnoses were made postoperatively. Endoscopic tattooing. EUS was routinely performed by 2 endosonographers before surgery. Endoscopy was performed using an Olympus UCT 140 linear echoscope (Olympus America Inc., Center Valley, PA). Once the lesion was identified, a 22-gauge EUS--fine needle aspiration needle (EchoTip Ultra; Wilson-Cook Medical, Winston-Salem, NC) was inserted 3--5 mm proximal to the lesion and 2--4 mL of sterile purified carbon particles (GI Spot; GI Supply, Camp Hill, PA) was injected under direct EUS visualization. Injection continued as the needle was withdrawn leaving an inked tract, with care taken to avoid peritoneal injection. Preprocedural antibiotics were given and continued for 3 days. Antibiotics were given after tattooing; however, we recognize that there are no data to support this practice and it has now been revisited. Laparoscopic distal pancreatectomy with and without spleen preservation. We begin by placing an umbilical port using a direct Hassan cut-down technique. Under direct visualization, we then insert 2 ports in the upper mid-line (or right of mid-line for more medial tumors) and 1 in the left lower quadrant. The precise location for these ports depends on the location of the tumor, the possibility of removing the spleen, and the patient’s body habitus. Once local landmarks are identified, the gastrocolic omentum and short gastric vessels are divided, followed by take-down of the splenic flexure of the colon to achieve wide visualization of the lesser sac. We stop the dissection once exposure is adequate and the tumor or tattoo is easily visible.
Fig 1. Illustration of the tattooing technique.
Once the tumor or tattoo is visualized, we mobilize the gland from its inferior border (Fig 2). The inferior approach facilitates dissection of the posterior aspect of the gland from the retroperitoneal bed. The splenic artery and vein branches can be visualized from underneath the pancreas, and we alternate dissection of the splenic vessels from above and below the gland because this exposure offers the best visualization. When splenic preservation is performed, the small branches of the splenic vessels to the pancreas parenchyma are individually dissected and divided; but when we include a splenectomy, we divide the splenic vessels individually with a gastrointestinal anastomosis stapler 2.5 mm (white vascular load) stapler. The gland is divided with an endogastrointestinal anastomosis stapler 2.5 or 3.5 mm (white vascular load or blue GI load) depending on pancreas thickness. The reticulating stapler is reinforced with a bioabsorbable staple line material. In patients with a pancreas tattoo, the pancreas is divided just proximal to the tattoo with a margin of $1 cm (Fig 3). Clear margins are confirmed on frozen section before closing. When there is a suspicion of malignancy or a technical reason necessitates removal of the spleen, we choose to mobilize the spleen after individual division of the splenic artery, vein, and gland. Statistical analysis. Fisher exact test was used to compare categorical variables, and the Wilcoxon rank-sum test was used to compare continuous variables because most variable did not appear to be normally distributed. Statistical analyses were performed with the use of SAS software, version 9.1 (SAS Institute Inc., Cary, NC). Results were considered significant if P < .05. RESULTS An endoscopically placed tattoo was performed preoperatively in 10 patients. The median time from tattooing to operative resection was 38 days (range,
Newman et al 373
Surgery Volume 148, Number 2
Fig 2. EUS FNA tattoo (white arrow) at laparoscopy.
1--83) before surgery. Tattooed and nontattooed patients were of a similar age and gender (Table I). Five of the tattooed resections were in the initial half of our experience with the procedure and the remaining 5 were in the latter half of our experience. Operative time was decreased in patients who had a preoperative tattoo because the tattoo was very useful in rapidly localizing the tumor and planning the line of resection (Table II). Median operative time was statistically significantly shorter in the tattoo group (128.5 vs 180 minutes in the nontattoo group; P = .01). All 10 tattoos were easily visible laparoscopically (Fig 1), including the tattoo placed 84 days before surgery. The median estimated blood loss was greater in the nontattoo group, although this was not significant using the Fisher exact test. (62.5 vs 10 mL in the tattooed group; P = .68). Two patients in the nontattoo group underwent a second operative procedure. The first required extension of the pancreatectomy, because no lesion was identified in the initial resection specimen and the second had postoperative bleeding that required reoperation. Postoperative morbidity, defined as any complication arising in the 30-day postoperative period, was 23% in the nontattoo group (n = 6) and 20% in the tattoo group (n = 2). There was 1 death in the nontattoo group (4%) owing to a postoperative arrhythmia that resulted in cardiac arrest. An extensive investigation revealed no evidence of anemia or cause related to the operative technique. Patients who had a laparoscopic resection with a tattoo had a decreased length of stay compared with nontattooed patients 4 days (range, 3--8) versus 5 days (range, 2--17), although this difference was not significant (P = .10). Major comorbidities were similar in both groups with a mean number of 1.1 major comorbidities in the tattoo group and 0.9 in the nontattoo group (P = .27). Histologic findings are shown in Table III. The most common indication for resection was a
neuroendocrine tumor, accounting for 50% (n = 5) of the tattoo cases and 31% (n = 8) of the nontattoo group. Adenocarcinoma accounted for 20% (n = 2) of the tattoo cases and 8% (n = 2) of the nontattoo group. Other lesions which were resected included serous cystadenoma, mucinous cystadenoma, intraductal papillary mucinous neoplasm and pancreatic pseudocyst. The median size of the tumor in the tattoo group was 0.7 cm smaller than in the nontattooed tumors (1.3 vs 2 cm; P = .04). One patient who was tattooed 12 hours before laparoscopy did demonstrate some mild pancreatitis. After this observation, we increased the time between tattooing and surgery to allow any such subclinical inflammation to resolve before operation. There were no other documented cases of acute pancreatitis in the patients who underwent EUS-guided tattoo placement on histology. DISCUSSION Laparoscopic distal pancreatectomy is increasingly being performed for tumors of the body and tail of the pancreas. Laparoscopic distal pancreatectomy was initially described by Gagner et al14 in 1996 for resection of pancreatic neuroendocrine tumors. Since then, there have been an increasing number of reports of laparoscopic distal pancreatectomy for a range of indications.9,15,16-39 Retrospective, case-control studies comparing laparoscopic distal pancreatectomy and open distal pancreatectomy have demonstrated significantly shorter hospitalization time for the laparoscopic group, with no significant difference in either operative time or rate of complications.1,13,17,40 Rationale of demarcation. One of the challenges faced by surgeons performing laparoscopic distal pancreatectomy is that lesions can be difficult to identify. Even lesions that are clearly visible
374 Newman et al
Surgery August 2010
Table I. Patient characteristics
Age at surgery, y (median, range) Male Female Time between EUS and LDP, days (median, range)
Tattoo group (n = 10)
Nontattoo group (n = 26)
60.5 (38–81)
61.5 (28–84)
4 (40%) 6 (60%) 38 (1–83)
12 (46%) 14 (54%) NA
EUS, Endoscopic ultrasound; LDP, laparoscopic distal pancreatectomy; NA, not applicable.
Fig 3. Resected specimen showing tattoo (white block arrow) proximal to the tumor (black thin arrow).
on imaging techniques may not be visible during laparoscopy as the lesion is deep in the parenchyma requiring palpation to localize.26 The challenge to appropriately localize small pancreatic tumors is not new to the era of laparoscopy. For example, small islet cell tumors of the pancreatic tail can be notoriously difficult to find using an open operative approach. Ultrasonography has been used in the past to locate pancreatic lesions intraoperatively and this technique has been used laparoscopically. We prefer tattooing pancreatic lesions over laparoscopic ultrasonography for many reasons. First, tattooing provides a more definitive localization in demarcating a line of resection. Studies have shown that intraoperative ultrasound has a sensitivity of 80--100%, although these studies use both palpation and ultrasound combined during open surgery. When ultrasound is performed laparoscopically, palpation is unavailable and the sensitivity of ultrasound is decreased.16,41-43 When attempted laparoscopically, an inability to localize with intraoperative ultrasonography can lead to conversion to open operation unnecessarily. In addition, laparoscopic ultrasound probes frequently do not provide the resolution of the standard intraoperative probes.2,16 Intraoperative ultrasound, either open or laparoscopic, may locate a tumor; however, it may not allow for precise marking in real time. Assessment of an intra-abdominal organ must be done in 2 separate planes to confirm a mass is really present. Also, visualization of the tattoo intraoperatively allows for directed dissection, limiting unnecessary exploration for the tumor and decreasing the risk of injury of surrounding structures. Tattooing also helps to ensure an adequate oncologic margin because the tattoo is
placed proximal to the lesion. Finally, we believe the precise localization offered by tattooing allows us to optimize the preservation of healthy pancreas parenchyma, mitigating the risk of future diabetes caused by unnecessary over-resection. Endoscopic tattooing of the pancreas was first described by Gress et al in 2002,11 who used India ink to identify an insulinoma before operative resection. After reports of complications associated with India ink, alternative methods of tattooing have been sought.44,45 There have been case reports of using indocyanine green ink,12 methylene blue,13 and GI spot10 to tattoo the pancreas, with no complications reported. EUS-guided fine needle aspiration is safe with a complication rate of 0--2.2%.46-49 Tumor seeding along the needle path is a potential complication of EUS-guided fine needle aspiration, however, it is very rare,50-52 with only 1 report of tumor seeding of a pancreatic adenocarcinoma.50 The risk of seeding with EUS-guided tattooing should be negligible, because the needle is placed proximal to, rather than within, the tumor. Another potential complication of endoscopic fine needle aspiration of the pancreas is pancreatitis with an incidence of 0--2% in the literature.46-49,53-55 There was no evidence of pancreatitis on histologic examination in our series. Endoscopic tattooing was performed a median of 38 days before laparoscopic distal pancreatectomy, with a range of up to 83 days. In all cases, the tattoo was clearly visible at laparoscopy (Fig 1). The importance of being able to identify the lesion is seen in this study where the lesion was identified and resected in all 10 tattooed patients. This contrasts with the nontattoo group, where 1 patient required a repeat operative procedure because an 8-mm insulinoma could not be visualized during laparoscopy. Intraoperative ultrasonography was performed during the first operative procedure and a small lesion identified in the tail of the
Newman et al 375
Surgery Volume 148, Number 2 Table II. Operative and postoperative details Tattoo group (n = 10) Operative procedure LDP Spleen-preserving LDP OR time, min (median, range) Estimated blood loss, mL (median, range) Conversion to open Complication rate Wound infection Pancreatic leak Abscess Postoperative bleeding Postoperative morbidity Time to discharge, days (median, range) Mortality
6 4 128.5 10
(60%) (40%) (53–180) (10–200)
Nontattoo group (n = 26) 17 9 180* 62.5
(65%) (35%) (120--240) (10–800)
0 (0%)
6 (23%)
0 2 0 0 2 4 0
1 4 0 1 6 5 1
(0%) (20%) (0%) (0%) (20%) (3–8) (0%)
(4%) (15.4%) (0%) (4%) (23%) (2–17) (4.5%)
Postoperative morbidity was defined as any complication arising in the 30-day postoperative period. *P < .05. NA, Not applicable.
Table III. Pathologic diagnosis in surgical resection specimen Tattoo group (n = 10)
Nontattoo group (n = 26)
Neuroendocrine 5 (50%) Adenocarcinoma 2 (20%) Serous cystadenoma 1 (10%) Mucinous cystadenoma 2 (20%) Chronic pancreatitis 0 IPMN 0 Pseudopapillary tumor 0 Size, cm (median, range) 1.3 (0.8–2.8) Node positive, n (%) 1 (12%)
8 (31%) 2 (8%) 5(19%) 3 (12%) 2 (8%) 4 (15%) 2 (8%) 2.0 (0.6–6.5) 2 (10%)
IPMN, Intraductal papillary mucinous neoplasm.
pancreas was resected. However, when the patient became hypoglycemic on postoperative day 3, it became apparent that this was a multifocal lesion and the preoperatively identified (by EUS) symptomatic lesion had not been resected. The patient then underwent endoscopic tattooing of the lesion, which was clearly visible on repeat laparoscopy and the lesion fully resected. Zografos et al13 reported a similar situation where a patient with a confirmed insulinoma found on EUS underwent laparotomy, but the lesion could not be identified despite the use of intraoperative ultrasound. Operative time. The median operative time was significantly greater in the nontattoo group 180 minutes (range, 120--240) versus 128.5 minutes (range, 53--180) in the tattoo group. This difference in operative times was significant (P = .01).
The results in both the nontattoo and tattoo groups are better than the literature, where the mean operative time is 220 minutes (range, 65-500).56 We believe the shorter operative time in the tattoo group is due to the ease with which the lesion was identified after tattooing. Unlike intraoperative ultrasonography, where lesions cannot be identified in 10--40% of cases,14,16,23,26,41 the lesion was identified in all 10 cases (100%) in this series. Median intraoperative blood loss was less in the tattoo group (10 vs 62.5 mL in the nontattoo group), although this was not significant (P = .68). This trend may have occurred because the tattoo spares unnecessary dissection. Postoperative morbidity and time to discharge were not different between the 2 groups. Preventing diabetes. Preservation of pancreatic parenchyma is an important goal of pancreas surgery. After distal pancreatectomy, 8--23% of patients develop new-onset diabetes.42,57 In addition, 61% will develop exocrine insufficiency after resection.42 Endoscopic tattooing allows the surgeon to precisely locate a lesion to within 3--5 mm, and could potentially limit the amount of pancreatic tissue resected. It is not possible to assess whether this is sufficient to affect the development of endocrine or exocrine pancreatic insufficiency in this retrospective study; larger, prospective studies are needed to examine this. Limitations. This study has several important limitations. It is a retrospective, single-center study based on the experience of 2 surgeons. There is a natural referral bias because patients who were
376 Newman et al
referred for EUS-guided tattooing had smaller tumors. In addition, it is difficult to control the many confounding variables that contribute to long operative times. Further studies are required to confirm the findings in this study. In conclusion, despite these limitations, the finding of decreased operative time is significant. We recommend endoscopic tattooing for patients undergoing laparoscopic distal pancreatectomy for tumors <4 cm. In our experience, tattooing decreases operative time and, more important, demarcates a precise line of resection to avoid the unnecessary resection of additional pancreatic parenchyma. We also believe that these findings are transferable to open operations in decreasing operative times by facilitating identification of small lesions. The authors thank Corrine Sandone for the artistic contributions to the manuscript and Mr and Mrs Chad and Nissa Richison for sponsoring this research. REFERENCES 1. Kooby D, Gillespie T, Nakeeb A, Hawkins W, et al. Left-sided pancreatectomy: a multicenter comparison of laparoscopic and open approaches. Ann Surg 2008;248:438-46. 2. Pryor A, Means JR, Pappas TN. Laparoscopic distal pancreatectomy with splenic preservation. Surg Endosc 2007;21: 2326-30. 3. Tang CN, Tsui KK, Ha JP, et al. Laparoscopic distal pancreatectomy: a comparative study. Hepatogastroenterology 2007;54:265-71. 4. Pierce RA, Spitler JA, Hawkins WG, et al. Outcomes analysis of laparoscopic resection of pancreatic neoplasms. Surg Endosc 2007;21:579-86. 5. Palanivelu C, Shetty R, Jani K, et al. Laparoscopic distal pancreatectomy: results of a prospective non-randomized study from a tertiary center. Surg Endosc 2007;21:373-7. 6. Baker MS, Bentrem DJ, Talamonti MS, et al. A prospective single institution comparison of peri-operative outcomes for laparoscopic and open distal pancreatectomy. Surgery 2009;146:635-45. 7. Finan KR, Cannon EE, Christein JD, et al. Laparoscopic and open distal pancreatectomy: a comparison of outcomes. Am Surg 2009;75:671-80. 8. Borja-Cacho D, Al-Refaie WB, Jensen EH, et al. Laparoscopic distal pancreatectomy. J Am Coll Surg 2009;209:758-65. 9. Jossart GH, Gagner M. Pancreaticoduodenal resection. J Hepatobiliary Pancreat Surg 2000;7:21-7. 10. Farrell JJ, Sherrod A, Parekh D. EUS-guided fine-needle tattooing for preoperative localization of early pancreatic adenocarcinoma. Gastrointest Endosc 2009;69:176-7. 11. Gress FG, Barawi M, Kim D, et al. Preoperative localization of a neuroendocrine tumor of the pancreas with EUS-guided fine needle tattooing. Gastrointest Endosc 2002;55:594-7. 12. Ashida R, Yamao K, Okubo K, et al. Indocyanine green is an ideal dye for endoscopic ultrasound-guided fine-needle tattooing of pancreatic tumors. Endoscopy 2006;38:190-2. 13. Zografos GN, Stathopoulou A, Mitropapas G, et al. Preoperative imaging and localization of small sized insulinoma with EUS-guided fine needle tattooing: a case report. Hormones (Athens) 2005;4:111-6.
Surgery August 2010
14. Gagner M, Pomp A, Herrera MF. Early experience with laparoscopic resections of islet cell tumors. Surgery 1996;120: 1051-4. 15. Cuschieri A, Jakimowicz JJ, van Spreeuwel J. Laparoscopic distal 70% pancreatectomy and splenectomy for chronic pancreatitis. Ann Surg 1996;223:280-5. 16. Jaroszewski DE, Schlinkert RT, Thompson GB, et al. Laparoscopic localization and resection of insulinomas. Arch Surg 2004;139:270-4. 17. Cuschieri SA, Jakimowicz JJ. Laparoscopic pancreatic resections. Semin Laparosc Surg 1998;5:168-79. 18. Patterson EJ, Gagner M, Salky B, et al. Laparoscopic pancreatic resection: single-institution experience of 19 patients. J Am Coll Surg 2001;193:281-7. 19. Fernandez-Cruz L, Herrera M, Saenz A, et al. Laparoscopic pancreatic surgery in patients with neuroendocrine tumours: indications and limits. Best Pract Res Clin Endocrinol Metab 2001;15:161-75. 20. Park AE, Heniford BT. Therapeutic laparoscopy of the pancreas. Ann Surg 2002;236:149-58. 21. Uranues S, Alimoglu O, Todoric B, et al. Laparoscopic resection of the pancreatic tail with splenic preservation. Am J Surg 2006;192:257-61. 22. Mabrut JY, Boulez J, Peix JL, et al. Laparoscopic pancreatic resection: a preliminary experience of 15 patients. Hepatogastroenterology 2005;52:230-2. 23. Mabrut JY, Fernandez-Cruz L, Azagra JS, et al. Laparoscopic pancreatic resection: results of a multicenter European study of 127 patients. Surgery 2005;137:597-605. 24. Misawa T, Shiba H, Usuba T, et al. Systemic inflammatory response syndrome after hand-assisted laparoscopic distal pancreatectomy. Surg Endosc 2007;21:1446-9. 25. Gramatica L Jr, Herrera MF, Mercado-Luna A, et al. Videolaparoscopic resection of insulinomas: experience in two institutions. World J Surg 2002;26:1297-300. 26. Ayav A, Bresler L, Brunaud L, et al. Laparoscopic approach for solitary insulinoma: a multicentre study. Langenbecks Arch Surg 2005;390:134-40. 27. Edwin B, Mala T, Mathisen O, et al. Laparoscopic resection of the pancreas: a feasibility study of the short-term outcome. Surg Endosc 2004;18:407-11. 28. D’Angelica M, Are C, Jarnagin W, et al. Initial experience with hand-assisted laparoscopic distal pancreatectomy. Surg Endosc 2006;20:142-8. 29. Dulucq JL, Wintringer P, Stabilini C, et al. Are major laparoscopic pancreatic resections worthwhile? A prospective study of 32 patients in a single institution. Surg Endosc 2005;19:1028-34. 30. Fernandez-Cruz L, Cosa R, Blanco L, et al. Curative laparoscopic resection for pancreatic neoplasms: a critical analysis from a single institution. J Gastrointest Surg 2007;11:1607-21. 31. Melotti G, Butturini G, Piccoli M, et al. Laparoscopic distal pancreatectomy: results on a consecutive series of 58 patients. Ann Surg 2007;246:77-82. 32. Han HS, Min SK, Lee HK, et al. Laparoscopic distal pancreatectomy with preservation of the spleen and splenic vessels for benign pancreas neoplasm. Surg Endosc 2005;19:1367-9. 33. Corcione F, Marzano E, Cuccurullo D, et al. Distal pancreas surgery: outcome for 19 cases managed with a laparoscopic approach. Surg Endosc 2006;20:1729-32. 34. Fernandez-Cruz L, Saenz A, Astudillo E, et al. Laparoscopic pancreatic surgery in patients with chronic pancreatitis. Surg Endosc 2002;16:996-1003. 35. Fabre JM, Dulucq JL, Vacher C, et al. Is laparoscopic left pancreatic resection justified? Surg Endosc 2002;16:1358-61.
Surgery Volume 148, Number 2
36. Vezakis A, Davides D, Larvin M, et al. Laparoscopic surgery combined with preservation of the spleen for distal pancreatic tumors. Surg Endosc 1999;13:26-9. 37. Van Nieuwenhove Y, Vandaele S, Op de Beeck B, et al. Neuroendocrine tumors of the pancreas. Surg Endosc 2003;17: 1658-62. 38. Berends FJ, Cuesta MA, Kazemier G, et al. Laparoscopic detection and resection of insulinomas. Surgery 2000;128: 386-91. 39. Briggs CD, Mann CD, Irving GR, et al. Systematic review of minimally invasive pancreatic resection. J Gastrointest Surg 2009;13:1129-37. 40. Larsen MH, Fristrup CW, Mortensen MB. Endoscopic ultrasound-guided fine-needle marking of a small pancreatic tumor. Endoscopy 2009;41(Suppl 2):E175-6. 41. Rosch T, Lightdale CJ, Botet JF, et al. Localization of pancreatic endocrine tumors by endoscopic ultrasonography. N Engl J Med 1992;326:1721-6. 42. Spitz JD, Lilly MC, Tetik C, Arregui ME. Ultrasound-guided laparoscopic resection of pancreatic islet cell tumors. Surg Laparosc Endosc Percutan Tech 2000;10:168-73. 43. Iihara M, Kanbe M, Okamoto T, Ito Y, Obara T. Laparoscopic ultrasonography for resection of insulinomas. Surgery 2001;130:1086-91. 44. Al-Haddad M, Wallace MB, Woodward TA, et al. The safety of fine-needle aspiration guided by endoscopic ultrasound: a prospective study. Endoscopy 2008;40:204-8. 45. Siddiqui UD, Rossi F, Rosenthal LS, et al. EUS-guided FNA of solid pancreatic masses: a prospective, randomized trial comparing 22-gauge and 25-gauge needles. Gastrointest Endosc 2009;70:1093-7. 46. Hikichi T, Irisawa A, Bhutani MS, et al. Endoscopic ultrasound-guided fine-needle aspiration of solid pancreatic masses with rapid on-site cytological evaluation by endosonographers without attendance of cytopathologists. J Gastroenterol 2009;44:322-8.
Newman et al 377
47. Fisher L, Segarajasingam DS, Stewart C, et al. Endoscopic ultrasound guided fine needle aspiration of solid pancreatic lesions: performance and outcomes. J Gastroenterol Hepatol 2009;24:90-6. 48. Paquin SC, Gariepy G, Lepanto L, et al. A first report of tumor seeding because of EUS-guided FNA of a pancreatic adenocarcinoma. Gastrointest Endosc 2005;61:610-1. 49. Doi S, Yasuda I, Iwashita T, et al. Needle tract implantation on the esophageal wall after EUS-guided FNA of metastatic mediastinal lymphadenopathy. Gastrointest Endosc 2008; 67:988-90. 50. Shah JN, Fraker D, Guerry D, et al. Melanoma seeding of an EUS-guided fine needle track. Gastrointest Endosc 2004;59: 923-4. 51. Iglesias-Garcia J, Dominguez-Munoz E, Lozano-Leon A, et al. Impact of endoscopic ultrasound-guided fine needle biopsy for diagnosis of pancreatic masses. World J Gastroenterol 2007;13:289-93. 52. Eloubeidi MA, Tamhane A. EUS-guided FNA of solid pancreatic masses: a learning curve with 300 consecutive procedures. Gastrointest Endosc 2005;61:700-8. 53. Yusuf TE, Ho S, Pavey DA, et al. Retrospective analysis of the utility of endoscopic ultrasound-guided fine-needle aspiration (EUS-FNA) in pancreatic masses, using a 22-gauge or 25-gauge needle system: a multicenter experience. Endoscopy 2009;41:445-8. 54. Fernandez-Cruz L, Saenz A, Astudillo E, et al. Outcome of laparoscopic pancreatic surgery: endocrine and nonendocrine tumors. World J Surg 2002;26:1057-65. 55. Gagner M, Pomp A. Laparoscopic pancreatic resection: Is it worthwhile? J Gastrointest Surg 1997;1:20-5. 56. Cho YB, Lee WY, Yun HR, et al. Tumor localization for laparoscopic colorectal surgery. World J Surg 2007;31:1491-5. 57. Lo CY, Lo CM, Fan ST. Role of laparoscopic ultrasonography in intraoperative localization of pancreatic insulinoma. Surg Endosc 2000;14:1131-5.