Surg Endosc (2014) 28:1641–1647 DOI 10.1007/s00464-013-3364-y

and Other Interventional Techniques

Premedication with erythromycin improves endoscopic visualization of the gastric mucosa in patients with subtotal gastrectomy: a prospective, randomized, controlled trial Byoung Yeon Jun • Myung-Gyu Choi • Jong Yul Lee • Myong-Ki Baeg Sung Jin Moon • Chul-Hyun Lim • Jin Su Kim • Yu Kyung Cho • In Seok Lee • Sang Woo Kim • Kyu Yong Choi



Received: 17 July 2013 / Accepted: 24 November 2013 / Published online: 1 January 2014 Ó Springer Science+Business Media New York 2013

Abstract Background Food residue in the remnant stomach after subtotal gastrectomy (STG) interferes with endoscopic observation. We investigated whether intravenous erythromycin improves gastric mucosa visualization in patients with STG. Methods This study was conducted from April 2012 to October 2012 as a double-blinded, placebo-controlled, randomized trial. Patients who received STG with complete resection (stage T1–2N0M0) were included. Exclusion criteria were diabetes mellitus, neurologic disease, myopathy, recent viral enteritis history, concomitant therapy influencing gastrointestinal motility and severe comorbidity. Patients were instructed to consume a soft diet for dinner between 1800 and 2000 h, and endoscopies were performed between 0900 and 1200 h. Patients were assigned randomly to receive either erythromycin (125 mg in normal saline 50 cc) or placebo saline. The endoscopy was performed 15 min after infusion. Grade of residual food was rated as follows: G0, no residual food; G1, a small amount of residual food; G2, a moderate amount of residual food; G3, a moderate amount of residual food that hinders observation of the entire surface, even with body rolling; G4, a great amount of residual food such that endoscopic observation is impossible.

B. Y. Jun (&)  M.-G. Choi  J. Y. Lee  M.-K. Baeg  S. J. Moon  C.-H. Lim  J. S. Kim  Y. K. Cho  I. S. Lee  S. W. Kim  K. Y. Choi Department of Internal Medicine, College of Medicine, The Catholic University of Korea, 505 Banpo-dong, Seocho-gu, Seoul 137-701, Republic of Korea e-mail: [email protected] M.-G. Choi e-mail: [email protected]

Results When good visibility was defined as G0?G1, visibility was significantly better in the erythromycin group (61 ? 19 %) than in the placebo group (38 ? 12 %, p \ 0.001). However, this effect was not seen in patients within 6 months after gastrectomy. The risk factor for food stasis in the placebo group (n = 58) was food stasis at last endoscopy. The only factor predicting erythromycin response in the erythromycin group (n = 56) was elapsed time since surgery. Adverse effects included nausea [11 (19.7 %)] and vomiting [1 (1.8 %)] in the erythromycin group and vomiting [3 (5.2 %)] in the placebo group. However, they were transient and tolerable. Conclusions Premedication with erythromycin improves mucosal visualization during endoscopy in patients with STG. (Clinical Trials registration number: NCT01659619). Keywords Erythromycin  Gastroparesis  Gastrectomy  Endoscopy

Postoperative surveillance of endoscopy is important for detecting missed synchronous and new metachronous cancers in patients after subtotal gastrectomy. The incidence of metachronous gastric cancer following distal gastrectomy has been reported as 1.1–6.0 %, with a median interval of 10–12 years from the initial surgery [1–3]. Food stasis is encountered frequently in the remnant stomachs of patients after subtotal gastrectomy (i.e., 9–42 % of cases) [4–7]. Food residues in the gastric remnant can interfere with accurate endoscopic observations, which hamper the early detection of carcinoma. A previous study demonstrated that meticulous follow-up examinations and the early detection of remnant gastric cancer may lead to a better prognosis [2]. Several methods have been tested to reduce gastric residues and facilitate better endoscopic

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viewing. Providing a soft diet before examination and [18 h fasting were required to obtain clear views, which was affected by patient compliance [6]. Instead of prolonging the fasting period, drinking 1 L of water after lunch on the previous day yielded better views. However, this method was insufficient because not all of the food residue was removed from the remnant stomach [7]. Erythromycin is a motilin agonist that induces immediate gastric contraction, which is similar to phase III contractions of the migrating motor complex (MMC) [8, 9]. Antroduodenal manometry has shown that erythromycin infusion produced contractions that propagated distally from the stomach to the small intestine within minutes [9], even in a patient with subtotal gastrectomy [10]. In previous studies, these contractions cleared residual blood and improved gastric mucosal examination in patients with acute upper gastrointestinal bleeding [11–15]. This effect of erythromycin has also been noted in patients with postoperative gastroparesis [10, 16–18]. Thus, the aim of our study was to determine whether intravenous erythromycin could reduce residual food levels and improve the quality of endoscopic viewing in patients with subtotal gastrectomy.

Patients and methods Inclusion and exclusion criteria Patients who received subtotal gastrectomy were invited to participate in this study, conducted at Seoul St. Mary’s Hospital between April 2012 and October 2012, if they had undergone surgery in the previous 5 years at surgical stages T1–2N0M0. Patients were excluded for the following reasons: (i) comorbidities such as diabetes mellitus, acquired immune deficiency syndrome, neurological disease (parkinsonism, multiple sclerosis, brainstem stroke or tumor, diabetic or amyloid neuropathy, or primary dysautonomias), scleroderma, and other connective tissue diseases; (ii) concomitant therapy with astemizole, dihydroergotamine, ergotamine, pimozide, terfenadine, narcotics, alpha-2adrenergic agonists, tricyclic antidepressants, calcium channel blockers, dopamine agonists, muscarinic cholinergic antagonists, octreotide, exenatide, glucagon-like peptide-1 agonists, or phenothiazines (although muscarinic cholinergic antagonists or agonists were not considered to affect gastrointestinal motility if patients had stopped taking them for at least 3 days); (iii) hypersensitivity to erythromycin or any component of the product; (iv) pregnancy or lactation. Study design This study was a prospective, randomized, doubleblind, placebo-controlled trial (Clinical Trials registration

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number: NCT01659619). Patients were instructed to consume a soft diet for dinner between 1800 and 2000 h, and endoscopies were performed between 0900 and 1200 h, such that their fasting times were shorter than 18 h at maximum. Patients were assigned to receive either erythromycin or placebo saline. Randomization was performed using computer-generated random numbers with sealed envelopes for concealed allocation and simple randomization. Treatments were delivered in a double-blind manner from the central pharmacy after computer-generated randomization of the assignment list. The treatment assignments were not released until the final analysis. Informed consent was obtained from each patient. Ethical approval for the study was granted by the institutional review board of Seoul St. Mary’s Hospital. The patients in the erythromycin group received an intravenous infusion of 125 mg erythromycin lactobionate in 50 mL of normal saline solution, whereas those in the placebo group received 50 mL of normal saline solution for 5 min. Endoscopy was performed 15 min after receiving the erythromycin or placebo infusion. Three surgeons performed endoscopies using an Olympus video endoscope GIF Q260 or H260 (Olympus, Tokyo, Japan) while blinded to the medication. The endoscopic findings of food stasis were reviewed and validated by an independent and blinded evaluation committee, which comprised two gastroenterologists (MC and BJ).

Outcome measurement The primary endpoint was the degree of food stasis. The amount of residual food was rated on a 5-point Likert scale as follows: grade 0, no residual food; grade 1, a small amount of residual food; grade 2, a moderate amount of residual food, but it was possible to observe the entire surface of the remnant stomach with body rolling; grade 3, a moderate amount of residual food, which hindered observation of the entire surface even with body rolling; and grade 4, a large amount of residual food, which made endoscopic observation impossible [19]. Good visibility was defined as grade G0 ? G1, and grades G2–4 indicated poor visibility. The factors that affected food stasis, and the effects and safety of erythromycin, were investigated. Gender, age, body mass index (BMI), time elapsed after surgery, food stasis at last endoscopy, history of abdominal surgery, method of surgery (laparoscopy vs. open), and method of anastomosis were analyzed in patients with good visibility and poor visibility. Before endoscopy, all patients were asked to complete the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire (EORTC QLQ-STO22) to assess their quality of life.

Surg Endosc (2014) 28:1641–1647

Statistical analysis The number of patients was calculated to satisfy the primary endpoint of the trial. A preliminary survey (unpublished data in this institution) found that 40 % of patients who had received subtotal gastrectomy in the previous 5 years had poor visibility at the time of endoscopy. We hypothesized that erythromycin might improve endoscopic visualization by reducing the poor visibility from 40 to 20 % (a error = 0.05; b error = 0.2) [20]. Thus, we calculated that 58 patients needed to be included in each group. Comparisons between groups were performed using Pearson’s v2 test for categorical variables (or Fisher’s exact test, if appropriate) and Student’s t test for continuous variables. Using multiple logistic regression analysis, we tested the factors associated with food stasis and the effects of erythromycin. p \ 0.05 was considered statistically significant. Analyses were performed using SPSS version 14 (IBM, Armonk, NY, USA).

1643 Table 1 Patient characteristics Variables Male gender, n (%)

Erythromycin (n = 56) 37 (66.1)

Age, year, mean (SD)

56.6 (10.3)

BMI (kg/m2), mean (SD)

21.7 (2.7)

Placebo (n = 58)

p value

36 (62.1)

0.39

59 (11.6)

0.17

21.1 (2.1)

0.22

T stage, n (%)

0.44

T1

52 (92.9)

55 (94.8)

T2

4 (7.1)

2 (3.4)

Time elapsed after surgery, months, mean (SD) Food stasis of the last endoscopya, n (%)

19.9 (16.1)

21.9 (16.1)

0.51

18/42 (42.9)

26/50 (52.0)

0.38

Method of anastomosis, n (%)

0.44

Billroth I

9 (16.1)

15 (25.9)

Billroth II

43 (76.8)

39 (67.2)

Rouxen-Y

4 (7.1)

4 (6.9)

Open surgery

27 (48.2)

21 (36.2)

Laparoscopy

29 (51.8)

37 (63.8)

Method of surgery, n (%)

Results In total, 116 patients were enrolled and randomized over 6 months, 114 of whom provided outcome data. One patient had a protocol violation due to insufficient waiting time after infusion while another in the erythromycin group withdrew consent. The final analysis comprised 56 patients in the erythromycin group and 58 in the placebo group. There were no significant differences in terms of gender, age, BMI, T stage, time elapsed after surgery, method of anastomosis, method of surgery, or history of abdominal surgery. The symptoms of patients did not differ according to the total EORTC QLQ-STO22 scores for the two groups (Table 1). The number of patients with good visibility was higher in the erythromycin group than in the placebo group (p \ 0.001, Fig. 1). In the placebo group, patients with good visibility (n = 29) and poor visibility (n = 29) were compared to determine the risk factors for food stasis. According to the univariate analysis, time elapsed after surgery and food stasis at the last endoscopy were risk factors for food stasis. However, food stasis at the previous endoscopy was the only significant risk factor for food stasis according to the multivariate analysis (Table 2). The factors predicting the erythromycin response were analyzed in the erythromycin group. Time elapsed after surgery, method of surgery, and method of anastomosis were associated with the erythromycin response according to the univariate analysis. However, time elapsed after surgery was the only significant factor that predicted the erythromycin response (Table 3). As time elapsed after surgery was the only factor that predicted the erythromycin response, the grade of food stasis was plotted against the time elapsed after surgery in Fig. 2. Premedication with erythromycin improved endoscopic

History of abdominal surgeryb, n (%) EORTC QLQ-STO22 questionnairec, mean (SD), total score

0.19

6 (10.7%) 189 (118)

6 (10.3%) 148 (117)

0.95 0.06

BMI body mass index, EORTC QLQ-STO22 European Organization for Research and Treatment of Cancer Quality of Life Questionnaire, SD standard deviation a

Patients who received first endoscopy after gastrectomy were excluded

b

Cholecystectomy, appendectomy, cesarean section, laparoscopy for uterine myoma removal, hysterectomy, and colectomy are included

c

EORTC QLQ-STO22 responses were linearly transformed to scores from 0 to 100 according to EORTC scoring manuals

visibility significantly in most patients who underwent endoscopy 6 months after surgery, but this effect was not seen within 6 months of surgery. The adverse events included 11 (19.7 %) cases of nausea and one (1.8 %) case of vomiting in the erythromycin group, and three (5.2 %) cases of nausea in the placebo group. In the erythromycin group, two of the nausea cases (3.6 %) and the vomiting case were moderate to severe. However, they were transient and tolerable, and all patients completed their endoscopic examinations.

Discussion This prospective placebo-controlled trial was designed to determine the effects of erythromycin on food stasis in

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Fig. 1 The percentage of patients with good visibility in the placebo group and in the erythromycin group. G0 no residual food; G1 a small amount of residual food; G2 a moderate amount of residual food; G3 a moderate amount of residual food that hinders observation of the entire surface, even with body rolling; G4 a great amount of residual food such that endoscopic observation is impossible

patients with subtotal gastrectomy. Premedication with erythromycin improved mucosal visualization markedly during endoscopy in post-gastrectomy patients without significant adverse events. Our findings suggest that the routine use of erythromycin should be considered before follow-up endoscopy in patients with subtotal gastrectomy. The reported frequency of postoperative gastroparesis varies depending on the characteristics of patients, their preparation method, and the definition of gastroparesis in different studies. A study of patients who had received

surgery up to 20 years previously reported a gastroparesis frequency of 18.7 % [4]. Risk factors for postoperative gastroparesis included systemic diseases such as endocrine, metabolic, and connective tissue disease, type of reconstruction, diet preparation, and immediate postoperative gastric retention. In a cohort of patients within 2 years of surgery, the frequency of gastroparesis was 42.6 %, which did not differ according to the method of reconstruction [5]. A recent Korean study reported a rate of 9.4 % for endoscopic failures due to food stasis. These were associated with prior abdominal surgery, soft, or liquid diet, Billroth type II reconstruction, longer fasting time, and longer gastrectomy-to-endoscopy interval [6]. The frequency of gastroparesis in this study was 50 % in the placebo group, which seemed to be higher than in other studies. This may have been because of the higher number of patients with a short gastrectomy-to-endoscopy interval, which is a factor known to affect postoperative gastroparesis. The Likert scale consists of subjective categories and can influence the relative frequency, although it was applied consistently. In addition, patients were permitted to have dinner on the day before the endoscopy in order to reduce their discomfort. There is no satisfactory preparation method for reducing the amount of food residue before endoscopic examination in distal gastrectomy patients. Diet modification is usually recommended to reduce food residues. Fasting for [18 h with a soft or liquid diet was significantly associated with fewer examination failures [6]. A preparation method that

Table 2 Univariate and multivariate analysis of risk factors for poor visibility, placebo group Factors

Poor visibility (n = 29)

Good visibility (n = 29)

OR (95 % CI)

p value

0.11

Univariate analysis Male gender, n (%)

15 (51.7)

21 (72.4)

0.41 (0.14–1.22)

Age, year, mean (SD)

56.7 (12.4)

62.2 (10.4)

0.96 (0.91–1.01)

0.079

BMI, kg/m2, mean (SD)

21.2 (2.3)

21.0 (2.0)

1.04 (0.81–1.33)

0.77

1.4 (1.1)

2.2 (1.5)

0.61 (0.39–0.95)

0.027

17/24 (70.8)

9/26 (34.6)

3 (10.3) 21 (72.4)

3 (10.3) 16 (55.2)

9 (31.0)

6 (20.7)

Billroth II (vs. Billroth I)

17 (58.6)

22 (75.9)

0.52 (0.15–1.73)

0.28

Roux-en-Y (vs. Billroth I)

3 (10.3)

1 (3.4)

2.00 (0.17–24.10)

0.59

1.00 (1.00–1.01)

0.34

Time elapsed after surgery, year , mean (SD) a

Food stasis of the last endoscopy , n (%) History of abdominal surgery, n (%) Laparoscopy (vs. open surgery), n (%)

4.59 (1.39–15.20)

0.012

1.00 (0.18–5.42) 2.13 (0.71–6.37)

1.00 0.18

Method of anastomosis, n (%) Billroth I

EORTC-STO22 total score, mean (SD)

162.7 (133.4)

133.1 (97.5)

Multivariate analysisa Time elapsed after surgery, year, mean (SD)

0.97 (0.92–1.01)

0.14

Food stasis of the last endoscopy, n (%)

3.49 (1.00–12.2)

0.05

BMI body mass index, CI confidence interval, EORTC QLQ-STO22 European Organization for Research and Treatment of Cancer Quality of Life Questionnaire, OR odds ratio, SD standard deviation a

Patients who received first endoscopy after gastrectomy were excluded

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Table 3 Univariate and multivariate analysis of factors predicting the effect of erythromycin, erythromycin group Factors

Poor visibility (n = 11)

Good visibility (n = 45)

OR (95 % CI)

p value

6.67 (0.78–56.69)

0.08

Univariate analysis Male gender, n (%)

10 (90.9)

27 (60.0)

Age, mean (SD)

57.2 (8.2)

56.4 (10.8)

1.01 (0.99–1.08)

0.83

BMI, kg/m2, mean (SD)

22.0 (2.5)

21.6 (2.8)

1.05 (0.83–1.33)

0.71

0.3 (0.4)

Time elapsed after surgery, year, mean (SD)

2.0 (1.3)

0.04 (0.005–0.38)

0.004

History of abdominal surgery, n (%)

3 (27.4)

3 (6.7)

5.25 (0.89–30.82)

0.07

Laparoscopy (vs. open surgery), n (%)

9 (82.8)

20 (44.4)

5.63 (1.09–29.00)

0.04

Billroth I

4 (36.4)

5 (11.1)

Billroth II (vs. Billroth I)

5 (45.5)

38 (84.4)

0.16 (0.33–0.82)

0.03

Roux-en-Y (vs. Billroth I)

2 (18.2)

2 (4.4)

1.25 (0.12–13.20)

0.85

1.00 (0.99–1.00)

0.17

0.04 (0.005–0.38) 1.25 (0.11–14.00)

0.004 0.86

Billroth II vs. Billroth I

0.80 (0.11–5.90)

0.83

Roux-en-Y vs. Billroth I

1.43 (0.079–25.80)

0.81

Method of anastomosis, n (%)

EROTIC-STO22 total score, mean (SD)

144.7 (72.4)

200.0 (125.0)

Multivariate analysis Time elapsed after surgery, year, mean (SD) Laparoscopy (vs. open surgery), n (%) Method of anastomosis, n (%)

BMI body mass index, CI confidence interval, EORTC QLQ-STO22 European Organization for Research and Treatment of Cancer Quality of Life Questionnaire, OR odds ratio, SD standard deviation

required 1 L water intake after lunch with prolonged fasting was compared with prolonged fasting in patients who had a moderate to large amount of food in their remnant stomach at the previous endoscopy 1–2 weeks earlier. The proportion with successful preparation was significantly higher in the water intake group than in the prolonged fasting group. However, the patients had to endure the discomfort of a long fast [7]. Hypothetically, prokinetics may be effective for the preparation of postoperative gastroparesis patients. However, no controlled trials have tested prokinetics. Cisapride was reported to improve the delayed emptying of a semisolid diet after pylorus-preserving gastrectomy for early gastric cancer, but it was removed from the market [11]. In this study, we demonstrated that intravenous erythromycin significantly reduced food residue, which improved mucosal visualization. This effect was almost 100 % effective 6 months after surgery. This preparation was not complicated because long fasting periods were not required. No significant adverse events were related to erythromycin premedication. Only two patients reported moderate nausea and one patient experienced vomiting. These symptoms were transient and tolerable, and all patients completed their endoscopic examinations. The factors predicting erythromycin response were time elapsed after surgery, laparoscopic

surgery, and type of surgery, although time elapsed after surgery was the only factor according to the multivariate analysis. Erythromycin premedication almost completely emptied the remnant stomach of food in patients 6 months after surgery. This effect was not seen in patients within 6 months of surgery. This might be related to intrinsic and extrinsic neuronal denervation after surgery. A rat model used to investigate denervation sequelae associated with intestinal transplantation demonstrated that a low level of neural regeneration may begin to appear 6 months after denervation [21]. This observation may explain why erythromycin was ineffective within 6 months of gastrectomy. The appropriate dose of erythromycin for premedication before endoscopy has not been determined. In this study, a dose of 125 mg was administered intravenously 20 min before endoscopy. As a motilin agonist, low-dose erythromycin at 1–3 mg/kg stimulates antral contractions similar to phase III contractions of the MMC [8–10]. An acetaminophen emptying test using healthy volunteers demonstrated that a dose of 3 mg/kg erythromycin had the most powerful effect on gastric clearance but more frequent adverse events than 1.5 mg/kg [22]. High doses of 1,000 mg oral erythromycin were compared with a 250 mg dose in diabetic gastroparesis patients, but gastric emptying did not improve, and side effects increased with the higher

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Fig. 2 The grade of food stasis against the time elapsed after surgery in the placebo group and in the erythromycin group

dose [23]. In critically ill and ventilated patients, erythromycin doses as low as 70 mg were as effective as 200 mg doses in promoting gastric emptying [24]. A dose of 250 mg was administered in most previous studies of erythromycin for acute upper gastrointestinal bleeding [12– 14], but a dose of 125 mg was not less effective than 250 mg [11]. In previous erythromycin studies of acute gastrointestinal bleeding, endoscopy was performed 20–30 min after erythromycin infusion [11, 12, 14]. In human manometric studies, the first contraction was shown to be initiated and propagated distally within minutes of infusion, and lasted 15–25 min [10, 25]. One limitation of this study is the exclusion of patients with comorbidities. Those comorbidities are the

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risks of postoperative gastroparesis, such that the prokinetic effect of erythromycin on endoscopic mucosal visualization also needs to be verified in those patients. In conclusion, premedication with erythromycin improves mucosal visualization during endoscopy in patients with subtotal gastrectomy. Our findings suggest that premedication with a low dose of erythromycin should be considered before follow-up endoscopy in patients with subtotal gastrectomy. Acknowledgments This study was supported by Business of Globalization for Science and Technology funded by the Ministry of Education, Science and Technology, Seoul, Republic of Korea (Grant NRF-2011-0031644).

Surg Endosc (2014) 28:1641–1647 Disclosures Byoung Yeon Jun, Myung-Gyu Choi, Jong Yul Lee, Myong-Ki Baeg, Sung Jin Moon, Chul-Hyun Lim, Jin Su Kim, Yu Kyung Cho, In Seok Lee, Sang Woo Kim, and Kyu Yong Choi have no conflict of interest or financial ties to disclose

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Premedication with erythromycin improves endoscopic visualization of the gastric mucosa in patients with subtotal gastrectomy: a prospective, randomized, controlled trial.

Food residue in the remnant stomach after subtotal gastrectomy (STG) interferes with endoscopic observation. We investigated whether intravenous eryth...
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