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Home , Gastroparesis, Hernia repair, Nissen fundoplication, Vagotomy

Surgical (2019) 33:2620–2628 and Other Interventional Techniques https://doi.org/10.1007/s00464-018-6562-9

Impact of vagus integrity testing on surgical management in patients with previous operations with potential risk of vagal injury

Kamthorn Yolsuriyanwong1,2 · Eric Marcotte1 · Mukund Venu3 · Bipan Chand1

Received: 27 July 2018 / Accepted: 21 October 2018 / Published online: 25 October 2018 © Springer Science+Business Media, LLC, part of Springer Nature 2018

Abstract Background Thoracic and foregut operations can cause vagal nerve injury resulting in delayed gastric emptying or gastro- . However, the cause of in these patients is not always from a vagal injury. We hypothesize that vagal nerve integrity (VNI) testing may better define who has vagal nerve dysfunction. This information may change subsequent operations. The aim of this study was to evaluate the impact of VNI testing in patients with prior thoracic or gastric . Methods From January 2014 to December 2017, patients who had previous operations with the potential risk of vagal injury and had VNI testing were reviewed. Excluded patients were those with no plan for a second operation or the second opera- tion was only for gastroparesis. The main outcome was the percentage of operations altered due to the results of VNI testing. Results Twelve patients (eight females) were included. Ages ranged from 37 to 77 years. VNI results were compatible with vagal injury in eight patients (67%). VNI test results altered subsequent operative plans in 41.7% (5/12). Pyloroplasty was done in addition to fundoplication in two patients. Plans for hiatal repair with or without redo-fundoplication in three patients were changed by an additional pyloroplasty in one patient and partial with Roux-en-Y reconstruction in two patients. All patients who had secondary surgery had resolution of symptoms and improvement in objective testing. Conclusion The addition of VNI testing in patients with a previous potential risk of vagal nerve injury may help the surgeon select the appropriate secondary operation.

Keywords integrity · Vagus nerve injury · Delayed gastric emptying · Gastroparesis · Postsurgical gastroparesis ·

Previous thoracic and foregut surgery can cause The most common procedures, which can lead to such an or vagus nerve injury, either accidentally or intended. injury, include fundoplication, lung or heart transplantation, esophageal, gastric, and [1–3]. Injury of the vagus nerve can result in delayed gastric emptying or * Bipan Chand gastroparesis. Gastroparesis is a syndrome of delayed gas- [email protected] tric emptying without mechanical obstruction [4]. Causes Kamthorn Yolsuriyanwong of gastroparesis can be idiopathic, -related, post- [email protected] surgery, medication-induced, associated with connective tis- Eric Marcotte sue diseases, neurologic diseases, metabolic abnormalities, [email protected] infections, and malignancy [5]. Postsurgical gastroparesis is Mukund Venu the third most common cause of gastroparesis and has been [email protected] reported in 3–17% of all diagnosed gastroparesis [5]. 1 Division of GI/Minimally Invasive Surgery, Department The cardinal symptoms of gastroparesis include , of Surgery, Loyola University Chicago Stritch School , early satiety, , post-prandial fullness, and of Medicine, 2160 South First Avenue, Maywood, IL 60153, upper [4]. If these symptoms occur in the USA case of previous thoracic or foregut surgery, the clinician 2 Department of Surgery, Songklanagarind Hospital, Prince should have a high suspicion of a possible vagal injury and of Songkla University, Songkhla, Thailand consider further investigations. 3 Division of and Nutrition, Loyola University Medical Center, Maywood, IL, USA

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However, patient presentations can vary from absence of the results of treatments as “resolved” if the patient had no subjective symptoms to severe symptoms with . subjective symptoms of the primary disease and no delayed Also these symptoms can mimic other conditions including gastric emptying on further objective tests. We defined gastroesophageal reflux disease (GERD) and functional dys- “improved” when the patient had fewer symptoms than the pepsia [6]. Patients with minimal symptoms or less degree of first visit and “stable” if they had no change in symptoms. gastroparesis symptoms may be neglected. If these patients undergo a subsequent gastric-related operation, a negative Patient assessment and care outcome may occur [7–9]. Moreover, the cause of gastroparesis in patients with prior Patients with prior thoracic/foregut surgery and any degree thoracic or foregut surgery is not always from vagal nerve of gastroparesis symptoms who had an indication for a sec- injury. It may be from preexisting diseases such as diabetes, ond operation were referred to a surgeon and assessed by postoperative medications or even idiopathic. It is necessary medical and surgical experts in gastrointestinal motility dis- to evaluate for vagus nerve integrity (VNI) to distinguish orders. The included assessments were a detailed history, vagal nerve injury from other causes in order to choose an physical examination, comprehensive metabolic panel, and appropriate treatment. investigations. Patients with symptoms of gastroparesis were Therefore, patients with previous thoracic and gastric investigated by upper endoscopy, esophageal motility, 24-h surgery who require a secondary gastric operation and have pH monitoring, and contrast imaging. The purposes of these any degree of gastroparesis symptoms should have a vagus investigations were to rule out other possible causes (e.g., nerve function evaluation. Currently, no study has reported GERD, mechanical obstruction, and other esophageal/gas- on the benefits of VNI testing on subsequent gastric surgery tric motility disorders). In order to confirm the diagnosis of in patients who have had prior thoracic and foregut surgery gastroparesis, a 4-h nuclear medicine gastric emptying study with delayed gastric emptying. We hypothesize that VNI (GES) was used. VNI was evaluated using the response of testing may help determine who has vagal nerve dysfunc- plasma pancreatic polypeptide to sham feeding to distinguish tion. These results can affect patient treatment by altering the vagal injury from other causes [10]. subsequent operation. The aim of this study was to evaluate the impact of VNI testing on subsequent surgical treatment Gastric emptying in patients with prior thoracic or gastric surgery.

Gastric emptying of solids was measured by radionuclide Materials and methods scintigraphy using technetium-99m (Tc99m) sulfur colloid. The solid meal consisted of four ounces of liquid egg whites This study was performed at a metropolitan academic scrambled with 1.0 mCi of Tc99m-sulfur colloid, two slices quaternary care center. We retrospectively collected and of white bread and 120 mL of water. After the patient com- reviewed data from January 2014 to December 2017 on pleted the meal, images were obtained at intervals over the patients who underwent VNI assessment. Patients were abdomen for 4 h. A geometric mean was obtained and the excluded if they did not have a previous surgical history activity within the was quantified using decay cor- of thoracic or foregut operation or other procedures with rection. Gastric emptying was considered normal if 30–90%, the potential risk of a vagus nerve injury (e.g., heart–lung < 60%, < 30%, and < 10% of gastric content remain in the transplantation, anti-reflux procedures, hiatal , stomach by 1–4 h, respectively [11]. bariatric surgery, other foregut operations, or endoscopic treatment of GERD) or did not have vagal nerve function Vagus nerve integrity tested. Data collected and analyzed were age, gender, previ- ous surgical procedures, clinical presentation, investigations VNI was measured indirectly by the response of plasma pan- performed, results of VNI assessment, secondary procedure creatic polypeptide to sham feeding [10, 12, 13]. Patients planned or performed, and the results of subsequent inter- were required to fast overnight or at least 8 h before starting vention. Primary outcomes were the number and percent- the test. Two samples of venous blood were obtained at 15 age of operations which were changed due to the results of and 30 min before feeding for the baseline measurement. the VNI test. Secondary endpoints were the percentage of Patients then underwent a standard sham feeding by chew- patients who had an absence of gastroparesis symptoms and ing and spitting out a standard hamburger over a 15-min overall outcome. The absence of gastroparesis symptoms time period. They were also instructed to avoid swallow- was defined as no presentation of cardinal symptoms of gas- ing any food or drink during the test. Four blood samples troparesis including nausea, vomiting, early satiety, bloating, were then obtained at 15, 30, 45, and 60 min after the feed- post-prandial fullness, or upper abdominal pain. We defined ing was complete. An increase of more than 50% in plasma

1 3 2622 Surgical Endoscopy (2019) 33:2620–2628 pancreatic polypeptide level within 30 min of sham feeding Discussion indicated a normal function of the vagus . This tech- nique was described by Balaji et al. [10] with a sensitivity Vagal nerve injury can occur after foregut and thoracic sur- of 83%, specificity of 92%, and a positive predictive value geries and may result in delayed gastric emptying. In our of 92% to identify intact vagus nerves. study, the most common previous potential surgical proce- dure was fundoplication with repair followed by bilateral lung transplantation. These procedures carry a Results risk for vagal nerve injury that results in various degrees of gastroparesis symptoms. Thirteen patients underwent the VNI test between January A literature review by van Rijn et al. [7] showed that the 2014 and December 2017. All patients had a previous his- prevalence of unintended vagal nerve injury after anti-reflux tory of thoracic or gastric surgery. However, one patient was surgery ranged from 10 to 42%. The prevalence of , excluded because the second operation was performed only nausea and vomiting was higher in the vagal nerve injury for gastroparesis and not for any other condition. Therefore, group than the vagal intact group. The same authors also 12 patients were included for analysis and the data are sum- reported the short- and long-term results after anti-reflux marized in Tables 1 and 2. surgery in patients with or without vagal nerve injury. There were eight females and four males with ages that Short-term results showed postoperative gastric emptying ranged from 37 to 77 years. The 4-h GES was performed in was significantly delayed in the vagus nerve injury group 11 patients and all had delayed gastric emptying. One patient compared with the vagus nerve intact group. Long-term out- did not undergo the GES due to no vagal response from the comes showed significantly less reflux control and higher VNI testing before undergoing the GES. The VNI results reoperation rate in the vagus nerve injury group (7/13 [54%]) were compatible with vagal nerve injury in eight patients versus the vagal intact group (9/58 [16%]) (p = 0.007) and (67%). most patients underwent reoperation because of recurrence Five patients had prior bilateral lung transplantation and of reflux [8]. In our study, patients with previous fundoplica- six patients had prior hiatal hernia repair and fundoplica- tion with hiatal hernia repair underwent a second operation tion. One patient had prior open hiatal hernia. Nine patients due to recurrent hiatal hernia, fundoplication related com- (75%) presented with reflux symptoms and eight patients plications, and GERD. (67%) had at least one symptom of gastroparesis. One lung The incidences of gastroparesis after lung or heart trans- transplantation patient had no symptoms but his lung biopsy plantation or both ranged from 8 to 83% [2, 14–16]. Injury of pathology showed chronic micro-aspiration with acute rejec- the vagal nerve during lung transplantation, which can result tion. Two out of eight patients (25%) who did not respond to in delayed gastric emptying and esophageal dysmotility, can the vagus nerve integrity test and 50% of those with vagal induce GERD with a high prevalence of reflux from 23 to nerve response had an absence of gastroparesis symptoms 73% [15, 17] and can develop an obliterative bronchiolitis at presentation. from aspiration. Berkowitz et al. [2] reported 44% of patients Overall, VNI testing changed operative plans in 41.7% with symptomatic gastroparesis developed obliterative bron- (5/12). In the group with no vagal response, operative plans chiolitis possibly due to micro-aspiration. A study from were changed in five out of eight patients (62.5%). Plans for Raviv et al. [18] also reported similar results. All patients fundoplication in two patients were modified by an addi- with lung transplantation in our study underwent a second tional pyloroplasty. The plans for hiatal hernia repair with or operation due to treatment of GERD and micro-aspiration. without redo-fundoplication in three patients were changed Our findings show that reflux and reflux-related com- by an additional pyloroplasty in two and gastrojejunostomy plications (i.e., micro-aspiration) were usually the reasons in one. However, two of these three patients had hiatal hernia for subsequent surgery. Delayed gastric emptying can be repair and partial gastrectomy with Roux-en-Y reconstruc- used to explain these findings. Prolonged gastric reten- tion in the final treatments. On the other hand, the patients tion can increase intragastric pressure and lead to reflux. A who responded to vagus nerve integrity test had no change study from Gourcerol et al. [19] showed that delayed gas- in operative plans. tric emptying was associated with an increased number of All patients who had secondary surgery had resolution daily and post-prandial liquid/mixed reflux events, a longer of symptoms and improvement in objective tests (i.e., signs bolus clearance time, and increased esophageal proximal of rejection or micro-aspiration in lung transplant patients). extension. A literature review from Emerenziani et al. [20] reported that delayed gastric emptying may increase less acidic reflux without an increase of acid gastroesophageal reflux. Therefore, a less acidic reflux does not produce

1 3 Surgical Endoscopy (2019) 33:2620–2628 2623 silent aspiration displaced tight wrap fundoplication tube tion Diagnosis (pre-vagus nerve integrity nerve Diagnosis (pre-vagus test) • Post pulmonary transplantation• Post with • Recurrent paraesophageal hernia• Recurrent paraesophageal secondary dysmotility to • Esophageal • Gastric secondary stenosis misplaced to and gastrojejunostomy post • Status • Recurrent GERD • Recurrent hiatal hernia • Recurrent paraesophageal hernia• Recurrent paraesophageal • Gastroparesis at early post transplanta post - at early • Gastroparesis • GERD • GERD dysmotility • Esophageal hiatal hernia The wrap appeared very tight and displaced into tight and displaced into very appeared The wrap at antrumthe thorax. Medium amount of food hernia and paraesophageal fundoplication wrap capsule of the gastric banding. Slipped Nissen leading to body of stomach fundoplication to of stomach and narrowing acute angle junction, no obstruction stomach the cardia, chronic , medium amount of the chronic cardia, in the stomach food esophageal emptying, dilated and tortuous emptying, esophageal obstruction junction outflow Investigations conducted Investigations • EGD: normal no no reflux, • UGIS: mild silent aspiration, • EMS: normal GERD for negative • pH impedance: no rejection with biopsy: • Bronchoscopy • EGD: moderately dilated esophageal lumen. dilated esophageal • EGD: moderately • UGIS: dilated esophagus secondary a tight to at fundoplication pressure • EMS: high wrap • EGD: narrowing of cardia secondary of cardia • EGD: narrowing the to at gastroesophageal • UGIS: mild narrowing • EGD: gastritis, medium amount of food in • EGD: gastritis, medium amount of food • EMS: normal GERD for positive • pH impedance: • EGD: hiatal hernia, disruption of the at wrap • UGIS: recurrent hiatal hernia • EGD: normal • UGIS: normal • EMS: normal GERD for positive • pH impedance: gastric emptying • GES: delayed no rejection with biopsy: • Bronchoscopy • EGD: paraesophageal hernia• EGD: paraesophageal hernia• UGIS: paraesophageal with delayed peristalsis with• EMS: failed esophagogastric • EGD: gastritis motility esophageal • EMS: ineffective GERD for positive • pH impedance: no rejection with biopsy: • Bronchoscopy emphysema repair withrepair mesh and Nissen fun - doplication and anterior and posterior gastroplexy and tube (TIF) doplication chronic hypersensitivity pneumonitis hypersensitivity chronic sarcoidosis Previous potential risk potential operations Previous • Bilateral lung transplantation• Bilateral due to • Laparoscopic paraesophageal hernia paraesophageal • Laparoscopic • Adjustable gastric banding (ABG) • Adjustable hiatal hernia of AGB, repair • Removal and gastrostomy • Gastrojejunostomy • Transoral incisionless fundoplication • Transoral and hiatal hernia repair • Undo-TIF • Nissen fundoplication • Redo-fundoplication • Hiatal hernia and Nissen fun - repair reason) (unknown • Gastrojejunostomy • Bilateral lung transplantation• Bilateral due to • Bilateral lung transplantation• Bilateral due to sensation malnutrition nal bloating bloating, reflux symptoms bloating, reflux Presentation Reflux symptoms Reflux Dysphagia, gastric fullness gastric Dysphagia, Intractable N/V, severe severe Intractable N/V, Reflux symptoms, abdomi - symptoms, Reflux Reflux symptoms, N/V, N/V, symptoms, Reflux Reflux symptoms, N/V symptoms, Reflux N/V, early satiety, abdominal satiety, early N/V, Reflux symptoms, cough symptoms, Reflux Gender F F M M F F M F 66 65 59 39 37 64 61 64 Age Patient characteristics, investigations and pre-vagus nerve integrity nerve diagnosis and pre-vagus test investigations characteristics, Patient 1 Table Patient number 1 2 3 4 5 6 7 8

1 3 2624 Surgical Endoscopy (2019) 33:2620–2628 reflux Diagnosis (pre-vagus nerve integrity nerve Diagnosis (pre-vagus test) • Malpositioned fundoplication with gastroparesis • Diabetic • Barrett’s esophagus • Barrett’s dysmotility • Esophageal • Hiatal hernia micro-aspiration • Chronic • Hiatal hernia • GERD • Recurrent hiatal hernia • GERD - symp GERD, confirming association between events and reflux toms large amount of food in the stomach amount of food large of the carina the up to level extending hernia the stomach Investigations conducted Investigations • EGD: malpositioned wrap, no hiatal• EGD: malpositioned wrap, hernia reflux • UGIS: gastroesophageal pathological for negative • pH impedance: gastric emptying • GES: delayed • EGD: Barrett’s esophagus without dysplasia, esophagus without dysplasia, • EGD: Barrett’s reflux gastroesophageal • UGIS: significant hiatal motility, esophageal • EMS: ineffective pathological GERD for negative • pH impedance: • EGD: hiatal hernia, medium amount of food in • EGD: hiatal hernia, medium amount of food reflux • UGIS: no gastroesophageal esophagus • EMS: hypercontractile GERD for positive • pH impedance: no rejection with biopsy: • Bronchoscopy • EGD: , hiatal hernia, gastritis size hiatal• UGIS: moderate hernia • EMS: normal GERD for positive • pH impedance: chronic obstructive pulmonary obstructive disease chronic interstitial pulmonaryinterstitial fibrosis Previous potential risk potential operations Previous • Nissen fundoplication • Hiatal hernia repair • Bilateral lung transplantation• Bilateral due to • Bilateral lung transplantation• Bilateral due to • Open hiatal hernia repair abdominal bloating (type 2 - gastro DM with diabetic paresis) ration from lung pathol from ration - no GI symptom ogy, controlled type 2 DM) controlled nal pain Presentation Reflux symptoms, N/V, N/V, symptoms, Reflux - micro-aspi chronic Positive Reflux symptoms (poor symptoms Reflux Reflux symptoms, abdomi - symptoms, Reflux Gender F M F F 73 66 60 77 Age (continued) 1 Table Patient number 9 10 11 12 diabetes DM diabetes disease, N / V nausea/vomiting, reflux GERD gastroesophageal manometry study, EMS esophageal study, contrast UGIS upper gastrointestinal EGD esophagogastroduodenoscopy, mellitus, GI gastrointestinal

1 3 Surgical Endoscopy (2019) 33:2620–2628 2625 Clinical outcome Resolved Resolved Resolved Stable symptoms Stable Resolved Resolved Dead from acute lung rejection Dead from Improved Improved Normal lung pathology n/a n/a Follow- up period (weeks) 8 24 16 8 12 8 16 44 104 112 n/a n/a Heineke-Mikulicz pyloroplasty with fundoplication mesh and redo-Nissen plus Heineke-Mikulicz pyloroplasty esophagojejunostomy reconstruction esophagojejunostomy - gastroje with RY and partial gastrectomy reconstruction junostomy with mesh and proximal gastrectomy with gastrectomy with mesh and proximal reconstruction esophagojejunostomy RY poor patient status) reflux symptoms and cough symptoms reflux with RY gastrojejunostomy bypass gastrojejunostomy with RY Final management Final Laparoscopic Nissen fundoplication plus Laparoscopic Laparoscopic paraesophageal hernia paraesophageal repair Laparoscopic Laparoscopic total gastrectomy with RY with RY total gastrectomy Laparoscopic Medical therapy due to refusing surgery refusing due to Medical therapy Laparoscopic hiatalLaparoscopic hernia with repair mesh Laparoscopic paraesophageal hernia paraesophageal repair Laparoscopic PEG-J (Do not perform following operation due to due to operation perform following (Do not Medical therapy due to improvement of improvement due to Medical therapy Medical therapy due to refusing surgery refusing due to Medical therapy Laparoscopic paraesophageal hernia paraesophageal repair Laparoscopic Scheduled for operation for Scheduled Scheduled for operation for Scheduled redo- ± hernia with repair mesh and redo- fundoplication - recon esophagojejunostomy RY struction and hiatal hernia with repair mesh hernia with repair mesh fundoplication gastrojejunostomy) bypass plus drainage procedure plus drainage RY gastrojejunostomy bypass gastrojejunostomy RY hiatal hernia repair hiatal hernia repair Management plan after vagus nerve nerve plan after vagus Management integrity test (1) Pyloroplasty (2) Laparoscopic redo-fundoplication (2) Laparoscopic (1) Pyloroplasty (2) Laparoscopic paraesophageal paraesophageal (2) Laparoscopic Laparoscopic total gastrectomy with total gastrectomy Laparoscopic (1) Pyloroplasty (2) Laparoscopic redo-fundoplication (2) Laparoscopic (1) Pyloroplasty (2) Laparoscopic redo-fundoplication redo-fundoplication (2) Laparoscopic (1) Laparoscopic paraesophageal paraesophageal (1) Laparoscopic (2) Drainage procedure (previous (previous procedure (2) Drainage PEG-J then follow by PEG-J then follow (2) Laparoscopic fundoplication (2) Laparoscopic (1) Pyloroplasty Laparoscopic RY gastrojejunostomy gastrojejunostomy RY Laparoscopic Laparoscopic redo-fundoplication redo-fundoplication Laparoscopic Laparoscopic hiatalLaparoscopic hernia with repair Laparoscopic fundoplication withLaparoscopic Laparoscopic fundoplication withLaparoscopic a ­ test percutaneous endoscopic gastrostomy with jejunal extension tube with jejunal extension PEG-J percutaneous endoscopic gastrostomy Roux-en-Y, VNI No response No No response No No response No No response No No response No No response No No response No No response No Responded Responded Responded Responded GES Delayed Delayed Not done Not Delayed Delayed Delayed Delayed Delayed Delayed Delayed Delayed Delayed prevention) repair withrepair - mesh and redo-fundopli cation - recon esophagojejunostomy RY struction hiatal hernia with repair mesh repair repair with - mesh ± redo-fundopli cation fundoplication plus pyloroplasty bypass plus drainage procedure plus drainage RY gastrojejunostomy bypass gastrojejunostomy RY hiatal hernia repair hiatal hernia repair Initial management plan (pre-vagus plan (pre-vagus Initial management integritynerve test) Laparoscopic fundoplication (reflux fundoplication (reflux Laparoscopic Laparoscopic paraesophageal hernia paraesophageal Laparoscopic Laparoscopic total gastrectomy with total gastrectomy Laparoscopic Laparoscopic redo-fundoplication Laparoscopic Laparoscopic redo-fundoplication and redo-fundoplication Laparoscopic Laparoscopic paraesophageal hernia paraesophageal Laparoscopic PEG-J then follow by laparoscopic laparoscopic by PEG-J then follow Laparoscopic RY gastrojejunostomy gastrojejunostomy RY Laparoscopic Laparoscopic redo-fundoplication redo-fundoplication Laparoscopic Laparoscopic hiatalLaparoscopic hernia with repair Laparoscopic fundoplication withLaparoscopic Laparoscopic fundoplication withLaparoscopic Patient management plans before and after vagus nerve integrity nerve and clinical outcomes and after final managements vagus test, plans before management Patient VNI test was measured indirectly by the response of plasma pancreatic polypeptide to sham feeding to the polypeptide of plasma pancreatic response by indirectly measured was VNI test

2 Table Patient number RY integrity, nerve VNI vagus study, GES gastric emptying a 1 2 3 4 5 6 7 8 9 10 11 12

1 3 2626 Surgical Endoscopy (2019) 33:2620–2628 esophagitis but it can induce other esophageal or extra- impaired children with delayed gastric emptying. A study esophageal symptoms. from Khajanchee et al. [30] showed that patients with The symptoms of a patient with delayed gastric emptying delayed gastric emptying who underwent Nissen fundopli- can vary from no symptoms to severe symptoms. Also, the cation only had the poorest control of reflux symptoms correlation between symptoms and the rate of gastric emp- and had a higher incidence of gas bloat, hyperflatulence, tying is poor. Some patients with markedly delayed gastric and abdominal pain or fullness or both when compared to emptying are asymptomatic [21–23]. Our study found that patients who underwent Nissen fundoplication with pylo- one-fourth of patients with non-response vagal integrity test- roplasty. A further study from Masqusi and Velanovich ing and half of the response patients were asymptomatic. [31] also showed that the addition of pyloroplasty to a fun- These results might be underestimated because some do not doplication in patients with gastroparesis and reflux disease routinely evaluate vagus nerve function before performing had a significant improvement of bloating symptoms and a subsequent operation. gastric emptying. Completion or subtotal gastrectomy with Several management strategies were used for patients Roux-en-Y reconstruction can be used cautiously in selected with gastroparesis. Medical management and pharmaco- patients with postsurgical gastroparesis [4]. A systematic therapy of gastroparesis are usually the first-line treatments. review from Jones and Maganti [32] showed that comple- Other methods include endoscopic intrapyloric botulinum tion gastrectomy seems effective by decreasing symptoms toxin injection, gastric electrical stimulation, and surgical in patients with postsurgical gastroparesis. Forstner-Barthell intervention. They are often considered for failed medica- [33] reported that two-thirds of patients with severe post- tions, severe symptoms, or refractory gastroparesis [4]. We vagotomy gastric stasis improved their health status while evaluated patients who required a second operation and maintaining body weight after gastrectomy. However, the selected surgical interventions (e.g., pyloroplasty or comple- authors also reported a high rate of 40% which tion or subtotal gastrectomy with Roux-en-Y reconstruction) included narcotic withdrawal syndrome (18%), (10%), when performing a concurrent treatment for reflux disease wound infection (5%), intestinal obstruction (2%), and anas- and vagal injury. However, we did not perform additional tomotic leak (5%). Moreover, Roux-en-Y reconstruction can surgical procedures in patients without vagus nerve injury be a treatment for patients with reflux symptoms and is an unless otherwise indicated. We waited for at least 6 months option for failed primary or reoperative anti-reflux surgery from the primary operation, in order to avoid unnecessary with a high rate of success [34]. In general, most patients in treatment. Patients with temporary vagus nerve damage or this study were educated and encouraged to have a Roux- neurapraxia and no other causes of delayed gastric empty- en-Y reconstruction. Besides postsurgical gastroparesis ing (e.g., medications) were identified during this evaluation treatment, Roux-en-Y reconstruction can be a treatment of phase. failed primary or reoperative anti-reflux surgery and can For intrapyloric botulinum toxin injection, two rand- prevent bile reflux. Due to high morbidity after Roux-en-Y omized, double-blind, placebo-controlled trials showed reconstruction, some patients chose the pyloroplasty. How- improvement of gastric emptying. However, symptoms ever, pyloroplasty can cause either bile reflux gastritis or improved similar to placebo [24, 25]. A systematic review bile reflux esophagitis, but bile reflux esophagitis can be from Bai et al. [26] concluded there was evidence to support prevented by fundoplication and bile reflux gastritis can be intrapyloric botulinum toxin injection for the treatment of treated with medications. Therefore, pyloroplasty or comple- gastroparesis. Regarding gastric electrical stimulation, an tion gastrectomy with Roux-en-Y reconstruction was consid- initial meta-analysis and systematic reviews from Chu et al. ered as our main treatment options. [27] showed that a response from gastric electrical stimu- VNI testing before the second gastric operation altered lation was less in postsurgical gastroparesis (vagal injury) the course of treatment in almost 40% of patients by chang- patients. Furthermore, a recent meta-analysis and system- ing or performing an additional procedure. This means that atic reviews from Levinthal and Bielefeldt [28] concluded nearly half of the patients gained benefits from VNI testing. that gastric electrical stimulation is not superior to sham Furthermore, due to the high percentage of asymptomatic intervention for gastroparesis. Based on the results of these patients in our study, we suggest evaluating vagus nerve studies, we did not use intrapyloric botulinum toxin injection function in all patients with previous operations with a high or gastric electrical stimulation in our patients with vagal risk of vagal injury when performing a subsequent gastric injury. surgery. Few studies have reported the results of additional surgi- This study has some limitations. This study was a ret- cal drainage procedures (e.g., pyloroplasty) when treating rospective study with a small number of patients and no primary reflux disease. Alexander et al. [29] reported that comprehensive assessment of symptoms either before or pyloroplasty in addition to Nissen fundoplication improved after treatment. Further, some patients did not complete the wrap failure or recurrent reflux outcomes in neurological all preoperative investigations and only a few patients had

1 3 Surgical Endoscopy (2019) 33:2620–2628 2627 objective evaluations after treatment. In addition, we did 4. Camilleri M, Parkman HP, Shafi MA et al (2013) Clinical guide- not evaluate small bowel transit in our study. Vagus nerve line: management of gastroparesis. Am J Gastroenterol 108(1):18– 37 (quiz 38) injury may cause prolonged small bowel transit time and 5. Bielefeldt K (2012) Gastroparesis: concepts, controversies, and lead to gastroparesis-like symptoms. Delayed small bowel challenges. Scientifica (Cairo) 2012:424802 transit might occur concomitant with gastroparesis in these 6. Hasler WL (2008) Gastroparesis–current concepts and considera- patients. However, the resolution of symptoms in all patients tions. Medscape J Med 10(1):16 7. van Rijn S, Roebroek YG, Conchillo JM et al (2016) Effect of who had secondary surgery for gastroparesis in our study vagus nerve injury on the outcome of antireflux surgery: an exten- leads us to believe that the symptoms and complaints were sive literature review. Dig Surg 33(3):230–239 limited to the stomach. Besides, if the prolonged small bowel 8. van Rijn S, Rinsma NF, van Herwaarden-Lindeboom MY et al transit time is diagnosed, the primary treatments will be (2016) Effect of vagus nerve integrity on short and long-term efficacy of antireflux surgery. Am J Gastroenterol 111(4):508–515 behavioral and diet modification and medical therapy for 9. Rebecchi F, Allaix ME, Giaccone C et al (2013) Gastric empty- delayed small bowel transit, but this result has no effect on ing as a prognostic factor for long-term results of total laparo- the treatment of gastroparesis. scopic fundoplication for weakly acidic or mixed reflux. Ann Surg 258(5):831–836; (discussion 836–837) 10. Balaji NS, Crookes PF, Banki F et al (2002) A safe and noninva- sive test for vagal integrity revisited. Arch Surg 137(8):954–958 Conclusions (discussion 958–959) 11. Abell TL, Camilleri M, Donohoe K et al (2008) Consensus recom- mendations for gastric emptying scintigraphy: a joint report of the Almost 40% of patients who had previous operations that American Neurogastroenterology and Motility Society and the may have led to vagal injury and required a second gastric Society of Nuclear Medicine. Am J Gastroenterol 103(3):753–763 12. Lovgren NA, Poulsen J, Schwartz TW (1981) Impaired pancre- operation obtained benefits from VNI testing by altering atic innervation after selective gastric vagotomy. Reduction of the the additional operation. Some patients with delayed gastric pancreatic polypeptide response to food and hypoglycemia. emptying can present without symptoms of gastroparesis. Scand J Gastroenterol 16(6):811–816 The addition of VNI testing can help select the appropriate 13. DeVault KR, Swain JM, Wentling GK et al (2004) Evaluation of vagus nerve function before and after antireflux surgery. J Gas- secondary procedure and should be performed in all patients trointest Surg 8(7):883–888 (discussion 888–889) who have had previous operations with the potential risk 14. Sodhi SS, Guo JP, Maurer AH et al (2002) Gastroparesis after of vagus nerve injury. A large prospective study should be combined heart and lung transplantation. J Clin Gastroenterol conducted to validate these findings. 34(1):34–39 15. Grass F, Schafer M, Cristaudi A et al (2015) Incidence and risk factors of abdominal complications after lung transplantation. Acknowledgements The authors would like to thank all staff person- World J Surg 39(9):2274–2281 nel of Loyola University Medical Center, Maywood, IL, U.S.A. who 16. Costa HF, Malvezzi Messias P, dos Reis FP et al (2017) Abdomi- helped with the data retrieval and provided the essential information. nal complications after lung transplantation in a Brazilian single We would also like to thank Mr. Glenn Shingledecker in the Office of center. Transplant Proc 49(4):878–881 International Affairs, Faculty of Medicine, Prince of Songkla Univer- 17. Mertens V, Dupont L, Sifrim D (2010) Relevance of GERD in sity for the proofreading and language support. lung transplant patients. Curr Gastroenterol Rep 12(3):160–166 18. Raviv Y, D’Ovidio F, Pierre A et al (2012) Prevalence of gastro- Compliance with ethical standards paresis before and after lung transplantation and its association with lung allograft outcomes. Clin Transplant 26(1):133–142 Disclosures Kamthorn Yolsuriyanwong, Eric Marcotte, Mukund Venu 19. 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