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Ann Thorac Surg 2005;80:443-447
© 2005 The Society of Thoracic Surgeons

Original article: General thoracic

Intrathoracic Gastric Emptying of Solid Food After Esophagectomy for Esophageal Cancer

Hyun-Sung Lee, MD a , Moon Soo Kim, MD a , Jong Mog Lee, MD a , Seok Ki Kim, MD b , Keon Wook Kang, MD b , Jae Ill Zo, MD, PhD a , *

a Center for Lung Cancer, Center for Clinical Services, Research Institute and Hospital, National Cancer Center, Goyang, Gyeonggi, Korea
b Center for Nuclear Medicine, Center for Clinical Services, Research Institute and Hospital, National Cancer Center, Goyang, Gyeonggi, Korea

Accepted for publication February 18, 2005.

* Address reprint requests to Dr Zo, Center for Lung Cancer, National Cancer Center, 809 Madu-dong, Ilsan-gu, Goyang, Gyeonggi, 411-769, Korea (Email: jaylzo{at}ncc.re.kr).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
BACKGROUND: Information on the function of the intrathoracic stomach after esophageal resection for esophageal cancer is limited. This study evaluated the factors affecting intrathoracic gastric emptying of solid food in patients who had undergone this surgery.

METHODS: Between February 2003 and August 2003, intrathoracic gastric emptying of solid food was evaluated by radioisotope in 56 of the patients who underwent esophageal replacement surgery with the stomach for esophageal cancer. The 50% gastric emptying time was categorized into three ranges: over 180 minutes was defined as delayed, within 180 minutes as intermediate, and when all the radioisotopes were dumped into the jejunum as rapid. The factors affecting the gastric emptying were analyzed.

RESULTS: In 6 out of 56 (10.7%) patients the radioisotope removal was too rapid to check the gastric-emptying time, and hence the analysis was performed in 50 patients. Twenty-one (37.5%) patients showed significantly delayed gastric emptying. The 50% gastric emptying time calculated by an exponential fitting method was 422 and 109 minutes in the delayed and intermediate groups, respectively. Age, the method of gastric drainage, and the stomach shape used did not affect the intrathoracic gastric emptying. Only the follow-up interval after surgery was a significant factor on gastric emptying (p = 0.024). The intrathoracic gastric emptying of solid food was more and more increased over time after surgery by regression analysis (p = 0.03).

CONCLUSIONS: The use of the intrathoracic stomach as an esophageal substitute had a significant effect on gastric emptying, with intrathoracic gastric emptying of solid foods immediately after esophagectomy being markedly prolonged in about 50% of patients. However, the intrathoracic gastric emptying significantly increased over time. Research is required into improving intrathoracic gastric emptying in the early period after esophagectomy.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Most surgeons use the stomach to restore gastrointestinal continuity after esophagectomy for esophageal cancers. The preparation of the stomach as an esophageal substitutes is, however, associated with substantial alterations: the blood supply is decreased by 10% to 20% due to the ligation of the left gastric and left gastroepiploic arteries; the gastric capacity and the parietal cell mass are reduced because of the partial resection of fundus and corpus; the innervation is changed as a result of complete vagotomy; the shape is altered due to stretching; and the organ is realigned from positive pressure in the abdomen to negative pressure in the thorax [1]. In addition, most surgeons routinely add gastric drainage procedures to prevent gastric stasis secondary to the incidental truncal vagotomy. These surgical procedures have serious effects on gastric secretion, motility, gastric emptying, and gastroesophageal and duodenogastric reflux.

The general opinion has been that the stomach as an esophageal replacement acts as an inert tube after an esophagectomy [2, 3], and that ingested food is emptied only by gravity [4, 5]. However, there is recent clinical and experimental evidence that the motor activity of the denervated stomach slowly recovers over time [6]. With the inherent technical difficulties of evaluating this inaccessible structure, the poor survival rate of patients with esophageal cancer, and the reluctance of patients and surgeons to participate in time-consuming investigations, it is not surprising that few studies have attempted to document the functional results of the intrathoracic stomach as an esophageal substitute. Furthermore, little is known about intrathoracic gastric emptying of a solid meal. The purpose of this study was to elucidate the factors affecting intrathoracic gastric emptying of solid food in an esophageal substitute after esophagectomy in esophageal cancer.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
Between March 2001 and August 2003, one hundred patients underwent esophagectomy with gastric pull-up reconstruction at the National Cancer Center in Korea. Postoperative mortality rate was 6%. The gastric emptying study was started in February 2003. We tried to measure the gastric emptying in 57 patients from February 2003 to August 2003. In only one patient did we fail to measure the gastric emptying, due to the stenosis of the anastomosis site. The gastric emptying time was measured with a radioisotope in 56 of the patients. We obtained informed consent from the patient or next of kin for measurement of gastric emptying time by radionuclide, although this study was not a prospective study after approval of the Institutional Review Board. Table 1 lists the patients’ characteristics.


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  		Table 1. Patients’ Characteristics a
 
Surgery
Most of the patients with esophageal cancer underwent transthoracic esophagectomy and systematic lymph node dissection with complete truncal vagotomy (Table 1). The gastric conduit was pulled up with the whole stomach or after gastric-tube formation. The gastric tube was constructed using linear stapling devices (TLC, Ethicon, Sweden) inserted into the lesser curvature 5 cm proximal to the pylorus. The patients had either manually sutured anastomoses in the neck or circularly stapled anastomoses at the apex of the right chest or at the neck. The esophageal hiatus provided sufficient space for three fingers to be inserted. Gastric drainage was performed routinely with finger disruption of the pylorus. After surgery, the patient was extubated at the operating room and transferred to the intensive care unit.

Dietary Modification
Esophagography was performed on postoperative day 7. Sips of water were allowed after confirming the absence of anastomosis leakage, and a full liquid diet was implemented on the following day. If the patient tolerated the liquid diet, the diet was changed to a soft-food diet. All diets were divided into at least six portions per day. We recommended that walking exercise should be performed soon after food was consumed. All patients received metoclopramide HCl (Macperan) and cimetidine (Himentin) postoperatively. This dietary modification was maintained for a month or as needed. Diet alteration to a regular diet was considered during the follow-up period according to the patient’s condition.

Radionuclide Investigation of Intrathoracic Gastric Emptying
Scintigraphy was performed in patients who had been fasting for at least 8 hours and were positioned standing in front of a gamma camera (ARGUS, ADAC, Milpitas, CA) connected to a microcomputer. The field of view included the throat and the upper abdomen. The investigation of gastric emptying began with the consumption of solid food labeled with 2 millicuries (mCi) of technetium (99m-diethylenetriaminepentaacetate [DTPA]). The 300-g meal comprised scrambled egg mixed with 2 mCi technetium (99m-DTPA, 50 grams), 200 grams of rice rolled with seaweed (a kind of sushi), and 50 grams of yogurt. Anterior images were taken within 1 minute of the completion of the meal (defined as time 0), and then at 20-minute intervals for the following 180 minutes. Between imaging periods, the subjects were allowed to sit or walk in an adjacent waiting area. Power exponential fitting was used to analyze the time-activity curve over the stomach and to calculate the 50% gastric emptying time. The time-activity curves were analyzed for residual activity. For evaluation of the gastric conduit, the interval from the onset of deglutition to the point when the conduit activity fell to 50% of the peak activity was measured. This was defined as the 50% gastric emptying time (T50). The T50 was categorized into three ranges: over 180 minutes was defined as delayed, within 180 minutes as intermediate, and when all the radioisotopes were dumped into the jejunum as soon as swallowed, as rapid (Fig 1).



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  		Fig 1. Radionuclide imaging of intrathoracic gastric emptying at 120 minutes. (A) Intermediate gastric emptying is defined as 50% gastric emptying within 180 minutes. (B) Delayed gastric emptying is defined as 50% gastric emptying taking more than 180 minutes. (C) Rapid gastric emptying is defined when the radioisotope was dumped into the small intestine immediately after swallowing a radiolabeled meal.

 
Statistics
Fisher’s exact test was applied to analyze countable variables. Student’s t tests were used to compare the gastric emptying data, and standard statistics software was used (SPSS V11.0 for Windows 98, SPSS, Chicago, IL). An overall probability value of p less than 0.05 was considered statistically significant. Variables found in univariate analysis to be significantly different among groups at the 5% level were entered into a logistic regression analysis.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Six of the 56 patients exhibited rapid gastric emptying and twenty-one patients (37.5%) showed delayed gastric emptying. Analysis was performed in 50 patients, except for six patients with rapid gastric emptying in whom gastric emptying could not be measured.

Mean gastric emptying ratio for 180 minutes was 54 ± 24.3% and T50 was 241 ± 244 minutes. Mean gastric emptying ratio for 180 minutes was 30.1% and 72.1% of patients in the delayed and intermediate groups, respectively. The T50 was 422 minutes in the delayed group and 109 minutes in the intermediate group. There were no significant differences between two groups in age, type of stomach, and the method of gastric drainage. Follow-up interval after surgery was only a significant factor affecting gastric emptying (Table 2).


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  		Table 2. Comparison of Gastric-Emptying Data (n = 50) a
 
Within 6 months, nineteen out of 41 (46.3%) patients showed significantly delayed gastric emptying, compared with two of fifteen patients over 6 months (Fig 2A). Gastric emptying began to show the significant differences more than 100 minutes after swallowing (Fig 2B). Pylorus balloon dilatation was performed in eight patients with delayed gastric emptying and dysphagia, with seven of these patients within 6 months. Follow-up gastric emptying was investigated in four of these patients: gastric emptying was significantly improved in two of them, but the other two showed no improvement.



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  		Fig 2. Gastric emptying with time. (A) Gastric-emptying rate of solid food after esophagectomy with follow-up time. Regression equation; Emptying % = 49.123 + 1.067 x interval (month), r2 = 0.094, p= 0.03. (B) Graphical distribution of radioisotope residual activity in the intrathoracic stomach over time. ≤ 6 months; {blacksquare} > 6 months.

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
Patients who have undergone an esophagectomy frequently suffer from early satiety, reflux, some degree of dumping, and swallowing difficulty. Most patients can consume a near-normal diet 1 year after surgery. However, a long-term follow-up showed a 62% incidence of postoperative symptoms although 84% of patients were able to maintain a normal diet and 87% returned to work [7]. Only a minority was completely symptom free 5 or more years after esophageal resection [8]. Delayed gastric emptying after gastric and esophageal operations occurs in up to 50% of patients [9–12]. Burt and colleagues [13] reported that when esophagectomy patients ingested a semisolid radiolabeled meal, approximately 88% of it was retained in the stomach after 90 minutes in a supine position. In contrast, when healthy volunteers ingested a radiolabeled meal, only 20% to 40% was retained at the same time [14, 15]. The delayed gastric emptying appears to be attributable to decreased reservoir functioning of the gastric body due to an impairment of the gastric adaptive relaxation by truncal vagotomy, a reduction in gastric volume, and decreased mixing by the antrum [12]. The present study suggests that early satiety is due to a marked delay in gastric emptying in patients undergoing esophagectomy, at least in the early postoperative period. Although previous studies [16–18] have shown a lack of correlation between gastrointestinal dysfunction symptoms and a poor emptying rate from the esophageal substitute, eight patients with delayed gastric emptying who suffered from dysphagia and chest tightness after meals needed pylorus balloon dilatation in this study.

Diarrhea has been ascribed to truncal vagotomy after esophagectomy, and usually resolves over time. Although patients had varying degrees of dumping syndrome (postprandial nausea, cramping, sweating, or diarrhea), these symptoms were usually controlled with dietary manipulation and medication. However, rapid gastric emptying did not always induce the dumping syndrome. In this study, just one of the six patients with rapid gastric emptying suffered from chronic diarrhea. Follow-up of this patient showed that intrathoracic gastric emptying had markedly improved after 6 months without diarrhea.

Gastrointestinal motor activity is controlled in a complex manner by extrinsic and intrinsic innervation, circulating hormones, myogenic characteristics, and external influences from the central nervous system [19]. It has been reported that the myenteric neurons play a pivotal role in the interactions between extrinsic and intrinsic nerves [20, 21]. After extrinsic denervation of the stomach by division of the vagus nerves in the chest and partial sympathectomy along the branches of the celiac axis in radical lymph node dissection, the gastric wall secretes less acid and intrinsic factor, the fundus does not relax completely at mealtimes, the antrum generates weaker contractions, and the gallbladder empties more slowly. Because the motor and secretory functions of the stomach are controlled within the myenteric and submucosal plexuses in the gastric wall, the stomach is capable of recovering its functions over time in parallel with the progressive disappearance of the initial ultrastructural changes in intramural ganglionic cells [6]. Early in the postoperative period, the gastric wall exhibits weak microcontractions at the pacemaker’s rate of about three cycles per minute [22, 23]. As time passes, the amplitude of contractions increases, and peristalsis and the three phases of the classic migrating motor complex spontaneously reappear. Such a motor reorganization depends on the myenteric plexus in the gastric wall, which is capable of acting as a local control center that coordinates contractions of muscle fibers [24]. These ganglionic cells can progressively and spontaneously express their inborn organizational potentials despite being disconnected from the central nervous system. This is true for both acid and intrinsic factor secretions and for antral contractility. However, recovery of these functions is a slow process that usually takes years to complete.

Nakabayashi and colleagues [25] reported that the interdigestive pyloric motor activity of the denervated intrathoracic stomach as an esophageal substitute begins to recover at 12 months after an esophagectomy. Moreover, the interdigestive gastric motility progressively returns to normal over time from the pylorus cephalad. These results are consistent with a report that the denervated whole stomach is a contractile organ when it acts as an esophageal substitute after an esophagectomy, indicating that in the long run ingested food is evacuated not only by gravity but also by gastric contractions [6]. Furthermore, the sensation of early fullness at meals immediately after surgery would be reduced, in the long run, as surgery-induced inflammation in the gastric wall diminishes. These reports support our results that intrathoracic gastric emptying improved significantly over time.

In conclusion, the intrathoracic gastric emptying of solid food was markedly prolonged immediately after esophagectomy, and then improved over time. The shape of the stomach and the method of gastric drainage procedure did not influence the intrathoracic gastric emptying. The gastric emptying of the intrathoracic stomach as an esophageal substitute was quite variable, and that of solid foods immediately after esophagectomy was markedly prolonged in about 50% of patients. However, only 2 out of 15 (13%) patients had delayed gastric-emptying time over 6 months, of which just one patient suffered from early satiety and dysphagia. This result would also be affected by individual dietary modification over time in terms of the type, frequency, and amount of food consumed. Good quality of life of long-term survivors after esophagectomy may depend on both dietary adaptation and the improvement of intrathoracic gastric motility itself. Scintigraphic evaluation of gastric emptying would help us correlate patient symptoms with alimentary function during follow-up after esophagectomy. In addition, gastric emptying should be correlated with other evaluations such as a manometry and 24-hour pH monitoring for more accurate functional evaluation of the intrathoracic stomach after esophagectomy. Moreover, attempts should be made to improve intrathoracic gastric emptying in the early periods after esophagectomy.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

  1. Holscher AH, Voit H, Buttermann G, Siewert JR. Function of intrathoracic stomach as esophageal replacement World J Surg 1988;12:835-844.[Medline]
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