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10.1245/ASO.2005.03.078
Annals of Surgical Oncology 12:222-227 (2005)
© 2005 Society of Surgical Oncology
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Original Article

Is Pylorospasm a Cause of Delayed Gastric Emptying After Pylorus-Preserving Pancreaticoduodenectomy?

Dong K. Kim, MD1,6, Alexander A. Hindenburg, MD2,6, Sushil K. Sharma, MD3,6, Chang Ho Suk, MD4,7, Frank G. Gress, MD5, Harry Staszewski, MD2,6, James H. Grendell, MD3,6 and William P. Reed, MD1,6

1 Department of Surgery, Winthrop-University Hospital, Mineola, New York 11501
2 Department of Hematology/Oncology, Winthrop-University Hospital, Mineola, New York 11501
3 Department of Gastroenterology, Winthrop-University Hospital, Mineola, New York 11501
4 Department of Gastroenterology, New York Hospital Queens, Flushing, New York 11355
5 Division of Gastroenterology, Duke University Medical Center, Durham, North Carolina 27710
6 School of Medicine, State University of New York at Stony Brook, Stony Brook, New York 11794
7 Weil Medical College, Cornell University, New York, New York 10021

Correspondence: Address correspondence and reprint requests to: Dong K. Kim, MD, 877 Stewart Avenue, Garden City, NY 11530, USA; E-mail: kimdongkyu{at}yahoo.com.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Delayed gastric emptying (DGE) occurs in 14% to 61% of patients after pylorus-preserving pancreaticoduodenectomy, but its pathogenesis is unclear. We hypothesized that DGE may be due to pylorospasm secondary to vagal injuries at operation and may be preventable by the addition of pyloromyotomy.

Methods: Patients operated on consecutively between April 2000 and August 2003 were studied. Pyloromyotomy was of the Fredet-Ramstedt type combined with antroplasty. DGE-free recovery was defined as tolerance of a diet for three successive days by postoperative day 8. The symptom of nausea was used as a basis for nasogastric tube removal and diet resumption. A gastric emptying test (GET) with solid food was obtained. Patients with difficulty swallowing were fed via a feeding tube.

Results: There were 47 patients. Two patients were excluded because of death (n = 1) and ileus with pancreatic fistula (n = 1). Diagnoses were pancreatic cancer (n = 23), chronic pancreatitis (n = 11), ampullary cancer (n = 5), mucinous cystic neoplasm (n = 5), and duodenal villous adenoma (n = 3). Median times to nasogastric tube removal, start of liquid diet, and start of solid diet were postoperative days 2, 3, and 5, respectively. Two patients had tube feedings. Preoperative GET was abnormal in 51% , and postoperative GET was abnormal in 37% . The average length of stay was 9.5 days (median, 7 days). DGE occurred in only one patient (2.2%). There were no late complications during a 6-month follow-up.

Conclusions: The addition of pyloromyotomy to pylorus-preserving pancreaticoduodenectomy is effective in preventing DGE. Results are supportive of the hypothesis that DGE may be caused by operative injuries of the vagus innervating the pyloric region.

Key Words: Delayed gastric emptying • Pylorus-preserving pancreaticoduodenectomy • Pylorus-preserving Whipple procedure


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The Whipple procedure exemplifies a complex surgical procedure in evolution. Since the early work of Kausch, Whipple, and Brunschwig,1–3 the procedure has undergone numerous modifications. One of the latest innovations is the pylorus-preserving pancreaticoduodenectomy (PPPD), first reported by Watson4 and then brought to renewed popularity by Traverso and Longmire.5 PPPD is more physiological in concept and is easier to perform technically, and it has been proven to be as effective as the standard Whipple procedure.6–11 However, PPPD is often complicated by delayed gastric emptying (DGE) during the recovery period after operation.6–15 In reporting DGE for the first time, Warshaw and Torchiana6 noted that seven of eight patients could not tolerate a regular diet until the 16th postoperative day. The pathogenesis of DGE is still not fully understood, and its treatment remains largely symptomatic. In this study, we investigated the hypothesis that, in some patients, DGE may be caused by pylorospasm secondary to inadvertent operative injuries of the branches of the vagus nerve innervating the pyloric region and that DGE may be preventable by the addition of pyloromyotomy.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients who were candidates for a standard Whipple procedure (pancreaticoduodenectomy [PD]) and who underwent operation consecutively between April 2000 and August 2003 form the basis of this prospective, nonrandomized study. The only criterion for selecting the PPPD with the addition of pyloromyotomy (PPPD-P) over PD was whether approximately 2 cm of the proximal duodenum could be preserved without compromising a curative resection. The technique of PPPD was basically the same as described in the literature, with minor modifications.5,6 The pancreatic and bile ducts were not stented. The end of the pancreatic remnant was anastomosed to the side of the proximal jejunum in a retrocolic fashion. Pyloromyotomy was of the Fredet-Ramstedt type combined with antroplasty.16 The final reconstruction of PPPD-P is shown in Fig. 1Go. A digital maneuver stretching the antropyloric muscles and keeping them taut by placing an index finger through the open duodenum was found helpful in performing pyloromyotomy (Fig. 2Go). Drains were not used after March 2003.



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  		FIG. 1. Reconstruction of pylorus-preserving pancreaticoduodenectomy with pyloromyotomy in a retrocolic fashion.

 


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  		FIG. 2. Muscle fibers are stretched and kept taut for pyloromyotomy by a digital maneuver.

 
Epoetin alfa was started with a priming dose 40,000 U, given preferably 5 to 7 days before surgery, followed by a daily dose of 10,000 U on postoperative day 0 to 3. Acid inhibitors, either an H2-receptor blocker or a proton pump inhibitor, and broad-spectrum antibiotics were routinely administered for the first four postoperative days. Metoclopramide was administered between postoperative day 1 and 3 as an antiemetic.

A nasogastric (NG) tube was inserted in the operating room and was removed on postoperative day 1 or 2 unless the patient was nauseated. After the NG tube was removed, patients were observed overnight for nausea or vomiting. Absent such symptoms, diet was started; first with clear liquids and then advanced on sequential days to full liquids and solids. Patients who had difficulty swallowing were fed via a feeding tube. An NG tube was reinserted for vomiting or epigastric distress. In the absence of other complications requiring in-hospital care, patients were discharged when a diet was tolerated sufficiently without any need of parenteral support for three successive days.

A gastric emptying test (GET) with solid food was obtained between preoperative days 1 and 5 and between postoperative days 6 and 8. A standardized meal was used that consisted of two eggs labeled with 500 µCi of 99mTc sulfur colloid, two pieces of bread, and one pat of butter. Abnormal values were defined as gastric retention of the test meal >55% at 2 hours.17,18

DGE in this study was defined as a failure in the absence of any attributable complications to tolerate oral feeding for three successive days by postoperative day 8. DGE-free recovery was defined as tolerance of at least a liquid diet for three successive days without any need for parenteral support for hydration or nutrition and then progression to a regular diet. Patients were followed up for a minimum of 6 months.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
There were 29 women and 18 men with ages ranging from 29 to 86 years (average, 63 years). Pathologic diagnoses were pancreatic ductal carcinoma in 23 patients, chronic pancreatitis in 11, ampullary carcinoma in 5, mucinous cystic neoplasm in 5, and duodenal villous adenoma in 3.

Operative and perioperative profiles are shown in Table 1Go. One patient died after surgery, for an operative mortality rate of 2.1%. The portal vein in this patient was involved by tumor and was resected, but later it became thrombosed and caused bowel infarction. One patient developed intra-abdominal abscesses that were probably associated with a pancreatic fistula. A computerized tomogram of the abdomen with oral contrast was negative for DGE. This patient was fed intravenously because of generalized debilitation. Because an evaluation of gastrointestinal functions in these two patients for the purpose of this study was not feasible, they were excluded from the analysis. Overall, 18 (38%) of 47 patients had one or more postoperative complications, and two patients were readmitted after discharge (Table 2Go).


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  		TABLE 1. Operative and perioperative profiles
 

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  		TABLE 2. Postoperative complications and readmissions
 
Median times to NG tube removal, start of liquid diet, and start of solid diet were postoperative days 2, 3, and 5, respectively (Table 3Go). The NG tube was reinserted in four patients: two on postoperative day 3 and two others on postoperative day 4. It was removed again on postoperative day 5 in three patients and on postoperative day 11 in one. Two patients were fed via a feeding tube starting on postoperative day 2 in one and postoperative day 3 in the other. One patient was an 83-year-old man with difficulty swallowing of unknown etiology. The other was a 78-year-old man with severe oropharyngitis. Both patients tolerated tube feeding well.


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  		TABLE 3. Dates of NG tube removal and diet resumption
 
Thirty-nine patients had preoperative GET, 35 had postoperative GET, and 34 had both. The rest refused the test, claiming that eggs made them nauseated. A preoperative test was normal in 19 patients and abnormal in 20. A postoperative test was normal in 22 patients and abnormal in 13. For patients with both tests, a change occurred from abnormal to normal in 12 and from normal to abnormal in 7, and no change occurred in the rest (both normal in 9 and both abnormal in 6).

One patient experienced persistent nausea and vomiting even with an NG tube in place until postoperative day 11. She was diagnosed with DGE, thus making the DGE rate 2.2% for the series. PPPD-P was performed in this patient for chronic pancreatitis with intractable pain. Her preoperative GET was abnormal, with 99% retention. This patient required colostomy 6 months later for narcotic-induced obstructive pseudomegacolon.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The incidence of DGE in PPPD is given as 14% to 61% in the literature.6–15 Although there seems to be an improvement in DGE rates over time, the problem posed by DGE has not gone away. This is despite improving perioperative care, decreasing surgical morbidities, and increasing availability of pharmacotherapeutic agents. Our findings suggest that the etiology of DGE may lie beyond the confines of operative techniques, the skills of the surgeon, or the degree of excellence in perioperative care: DGE may be a condition inherent to PPPD.

None of the posited mechanisms of DGE—such as coexisting postoperative complications, the position of gastrointestinal reconstruction, retrocolic or ante-colic, duodenal ischemia, motilin deficiency, and so on—fully explains DGE. A causal relationship between abdominal complications and DGE15,19 was refuted by Sohn et al.,19 who reported a DGE rate of 5% in 129 patients who required interventional radiology for the treatment of abdominal complications, as opposed to 10% in 932 patients who did not have such complications. Gastric atony due to decreased levels of circulating motilin was studied by using erythromycin, a motilin agonist.9 The incidence of DGE was reduced only to 19% with erythromycin, versus 30% without it. Similarly marginal improvements in DGE rates have been reported by the reconfiguring of gastrointestinal reconstruction. In this study, we propose a novel hypothesis of pylorospasm as a possible cause of DGE.

The major variables in this study, as compared with our historical controls and published reports, are the addition of pyloromyotomy and the use of epoetin alfa. As shown in Fig. 1Go, our operative techniques closely conformed, except for pyloromyotomy, to those of original publications on the subject.5,6 Metoclopramide and epoetin alfa were given during postanesthesia recovery and were discontinued after the first three postoperative days. These drugs have short half-lives, and their clinical effects would not be sustained without repeated dosing. Epoetin alfa may have played a role in preserving a sense of well-being by lessening anemia in some patients, but it would not have had any expected effects on gastrointestinal function. The use of epoetin alfa for surgical anemia is still investigational.20

Evaluation of the physiologic consequences of PPPD-P was diffcult because of (1) the side effects of postoperative chemoradiotherapy for patients with malignant disease or (2) residual pain and discomfort in patients with chronic pancreatitis. However, in any given clinical setting, the patients with PPPD-P did not do any worse than those with PD or PPPD during a 6-month follow-up. Twelve patients experienced some degree of DGE symptoms up to 8 weeks after discharge. Two had DGE symptoms over 6 months. Since the study closed, another nine patients have undergone PPPD-P, and they are doing just as well without DGE.

The definitions of DGE in the literature are different from author to author. For this reason, differing DGE rates in the literature seem to reflect the differences in definitions more than they reflect true differences in incidence. DGE in the 5 major series, each comprising ≥100 patients, is defined as follows: NG tube left in place for ≥10 days9; NG suction for ≥10 days or delay of regular diet until after postoperative day 1412; a meal consumption of less than a half-volume of rice porridge for a month13; requirement for parenteral nutrition, reinsertion of an NG tube for >5 days, or radiological confirmation of DGE14; or intolerance of a regular diet by postoperative day 10.15 None of these reports provides an adequate explanation as to how and why a given definition was chosen. In discussing the arbitrariness of the DGE definitions, Frey, a discussant of the article by Patel at al.,11 commented that, "If we use five days as our standard, we could have almost 95% DGE. If we went out to 20 days, the percentage would probably be about 5%."11 Clearly, there is a need for an objective and biologically based cutoff date for DGE diagnosis.

In the absence of any indisputable evidence to choose one date over others as a cutoff for DGE diagnosis, we decided to run a trial of removing the NG tube and starting a diet by using the symptom of nausea as a basis and clinical guide. The results show that the NG tube can be removed by postoperative day 3 in 93% of patients and that a diet can be started on the following day in 95% of them (Table 3Go). The amounts of 24-hour drainage before NG tube removal in these patients varied widely between 20 and 750 mL (average, 219 mL). The NG output in four other patients who needed NG tube reinsertion was between 100 and 650 mL (average, 383 mL). We adopted postoperative day 8 as the cutoff for DGE diagnosis because by this time, all but one patient tolerated at least a liquid diet for three successive days without any need of parenteral support for hydration or nutrition and then progressed to take a regular diet.

The antropyloric region is innervated by the gastric branches of the vagus running along the lesser curvature of stomach and by the hepatic vagal plexus running in the gastrohepatic omentum and the porta hepatis.21 These structures are routinely subjected to dissection and manipulations during the PPPD, thus exposing the nerves to potential operative damage. Any such injury to the vagal branches could effectively lead to a physiologic derangement similar to that seen with truncal vagotomy. Dragstedt and Schafer22 observed for the first time in 1945 that truncal vagotomy was complicated by DGE. It occurred in 3 (23%) of 13 patients who underwent operation for the treatment of peptic ulcer disease.22 For this reason, the addition of a gastric drainage procedure has become standard with truncal vagotomy.

The controversy concerning PPPD over PD as a preferred procedure is beyond the scope of the study. Nevertheless, we find PPPD simpler and easier to perform, with minimal morbidity. It is a natural and, perhaps, necessary evolution for an operative procedure as complex as PD to undergo certain modifications to fit the disease. For the selected patients, PPPD seems the procedure of choice, and much the same can be said about PD as well. An approach of one-procedure-fits-all may not be the best in managing a variety of pancreatic and peripancreatic diseases.

For a historical control, we conducted a retrospective review of the records of our patients who underwent PPPD and PD during the previous 5-year period (Table 4Go). There were 28 PPPD patients and 30 PD patients who were comparable with the patients in the current series and who were suitable for analysis. DGE was recorded as a complication in 7 (25%) of the 28 PPPD patients. This rate was reduced in the current series to 2.2%. In the same review, 5 (17%) of 30 PD patients were found to have DGE. Other investigators also reported DGE after PD, with incidences ranging from 12% to 45%.7,10–12 The antrum may be an integral part of gastric emptying.


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  		TABLE 4. Operative procedures and their DGE rates and LOS
 
In conclusion, this study demonstrates that PPPD-P is effective in preventing DGE in most patients. The results support our hypothesis that operative injuries of the vagal nerves innervating the pyloric region may be the cause of DGE in PPPD patients. This concept merits further investigation for validation.

Received for publication March 20, 2004. Accepted for publication November 12, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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