JOURNAL OF LAPAROENDOSCOPIC & ADVANCED SURGICAL TECHNIQUES Volume 24, Number 9, 2014 ª Mary Ann Liebert, Inc. DOI: 10.1089/lap.2014.0125

Incidence of Deep Vein Thrombosis and Thrombosis of the Portal–Mesenteric Axis After Laparoscopic Sleeve Gastrectomy Ena Alsina, MD,1 Jaime Ruiz-Tovar, MD, PhD,2 Maria Remedios Alpera, MD,1 Jose Gregorio Ruiz-Garcı´a, MD,3 Manuel Enrique Lopez-Perez, MD,4 Jose Francisco Ramon-Sanchez, MD,1 and Francisco Ardoy, MD1

Abstract

Background: Venous thromboembolism is the most common postoperative medical complication after bariatric surgery. Mortality associated with thromboembolic processes can reach up to 50%–75%. The aim of this study was to determine the incidence of deep vein thrombosis (DVT) and portal–splenic–mesenteric vein thrombosis (PSMVT) in our population undergoing laparoscopic sleeve gastrectomy (LSG) as the bariatric technique, with an anti-thromboembolic dosage scheme of 0.5 mg/kg/day 12 hours preoperatively and maintained during 30 days postoperatively. Patients and Methods: A prospective observational study was performed, including 100 consecutive patients undergoing LSG between October 2007 and September 2013. To determine the incidence of DVT and PSMVT, all patients undergo contrast-enhanced abdominal computed tomography (CT) and Doppler ultrasonography (US) of both lower limbs on the third postoperative month, whether they were asymptomatic or symptomatic. Results: Contrast-enhanced CT showed 1 case of PSMVT (1%). Two patients presented DVT in the right leg (2%). All the cases were asymptomatic. Conclusions: The incidence of PSMVT and DVT after LSG with a prophylactic low-molecular-weight heparin dose of 0.5 mg/kg/day and maintained during 30 days postoperatively is 1% and 2%, respectively. According to these results, a postoperative screening with Doppler US and/or contrast-enhanced CT seems to be unnecessary. Introduction

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ccording to the World Health Organization, there are 1.6 billion overweight and 400 million obese people worldwide.1,2 Bariatric surgery has demonstrated to be the most effective and sustainable method for the regulation of morbid obesity, superior to both pharmaceuticals and combinations of diet and lifestyle regimens.2 Laparoscopic sleeve gastrectomy (LSG) is a restrictive bariatric procedure involving subtotal gastric resection of the fundus and body to create a long, tubular gastric conduit constructed along the lesser curve of the stomach. It was originally described as a first-stage bariatric procedure followed by Roux-en-Y gastric bypass or duodenal switch in high-risk patients. But, because LSG has the advantage of being a less risky technique and achieving similar results in terms of weight loss and resolution of comorbidities, many surgeons have adopted LSG as a primary bariatric procedure.3–5

Venous thromboembolism is the most common postoperative medical complication after bariatric surgery. The incidence of deep vein thrombosis (DVT) after laparoscopic bariatric surgery is around 3%, and that of pulmonary embolism is lower than 1%. However, mortality associated with pulmonary embolism is estimated to be between 50% and 75%.6–9 Portal– splenic–mesenteric vein thrombosis (PSMVT) is considered a rare event after bariatric surgery, but in the last few years increasing numbers of case reports of PSMVT after bariatric surgery, especially after LSG, have been published.10,11 The etiology of PSMVT seems to be unclear, with the long operative time, the high intraabdominal pressures due to pneumoperitoneum, and the anti-Trendelenburg position during surgery being postulated as causal mechanisms. Between 5% and 15% of all cases of PSMTV develop a bowel ischemia, with mortality rates around 40%.12,13 PSMVT symptoms are vague and nonspecific. In fact, 50% are asymptomatic, especially after chronic thrombosis when

Departments of 1Radiology and 2Surgery, General University Hospital Elche, Alicante, Spain. Departments of 3Surgery and 4Radiology, National Obesity Center, Mexico City, Mexico.

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collateral veins have been developed. Only abdominal pain seems to be a constant symptom.10,11 Contrast-enhanced abdominal computed tomography (CT) is the gold standard method for the diagnosis of PSMVT, with an accuracy rate of 90%.11,12 To date, there is no consensus about antithromboembolic prophylaxis for patients undergoing bariatric surgery. Most groups defend an optimal dosage of low-molecular-weight heparins (LMWHs) of 0.5 mg/kg/day, but some authors report that this is an insufficient dose as these patients are at high risk of developing thrombotic events. The postoperative prolongation of the prophylaxis is also a debated issue, as some authors defend that a prolongation of 5–7 days is enough, whereas others report the need for maintaining it for 1 month, considering laparoscopic bariatric surgery as a highrisk procedure performed in high-risk patients.14 The aim of this study was to determine the incidence of DVT and PSMVT in our population undergoing LSG as the bariatric technique, with an antithromboembolic dosage scheme of LMWH at 0.5 mg/kg/day 12 hours preoperatively and maintained during 30 days postoperatively. Patients and Methods Patients

The study was conducted at the Obesity Units from the General University Hospital of Elche (Alicante, Spain) and the National Obesity Center (Mexico City, Mexico). A prospective observational study was performed, including 100 consecutive patients undergoing LSG between October 2007 and September 2013. Inclusion criteria were a body mass index (BMI) of q40 kg/m2 or a BMI of q35 kg/m2 with associated comorbidities, according to the World Health Organization criteria.1,2 Exclusion criteria were loss to follow-up and patients’ allergy to the iodine contrast, with renal failure or severe thyroid disorders, because the performance of a contrast-enhanced CT was contraindicated in these subjects. Patients receiving chronic treatment with anticoagulant agents or with a history of DVT or hypercoagulability state were also excluded. Preoperative evaluation

A multidisciplinary team, including surgeons, endocrinologists, endoscopists, anesthetists, psychiatrists, psychologists, and specialized nurses, performed a combined medical, nutritional, and endocrinological work-up to evaluate potential surgical candidates. Preoperative assessment included abdominal ultrasonography (US), upper gastrointestinal endoscopy, functional respiratory tests, and analytical evaluation of the nutritional status. Psychiatrists and psychologists assessed additional interviews to evaluate the implication of the patient in following a strict diet in the postoperative course. A dietician established a diet giving a total daily energy intake of 1200 Kcal, similar to what they have to follow after the operation. Patients with documented gastroesophageal reflux disease were excluded and selected for undergoing a malabsorptive procedure. As an antithromboembolic prophylaxis scheme, enoxaparin (0.5 mg/kg/day) was prescribed for 12 hours preoperatively and for maintenance administration of 30 days postoperatively. Intermittent pneumatic compression of the lower limbs was also used, intraoperatively and until the patients recovered normal mobility.

ALSINA ET AL. Surgical technique

A longitudinal resection from the angle of His to approximately 3–4 cm orally to the pylorus is performed using a 40French bougie inserted along the lesser curve. A staple line inversion is made with a continuous oversewing of polypropylene 3-0 before the bougie is extracted. The section with the stapler is not performed very tight to the dilator, and the inversion is used to adjust the suture to the tube size. The patients are discharged on a liquid diet for 1 postoperative week, then transitioned to half-solid food for the following 3 weeks, and then progress to regular meals under specific dietary instructions for a daily intake of 1200 Kcal. Postoperative evaluation of thrombosis

The incidence of DVT and thrombosis into the portomesenteric axis is determined by systematic performance of Doppler US of both lower limbs and contrast-enhanced abdominal CT on the third postoperative month. In cases of suggestive symptoms, the tests were performed before this period. Doppler US was performed with a Toshiba Xario device (Toshiba Medical Systems Corp., Minato-Ku, Japan) and a lineal probe of 7.5–10 MHz. Common, deep, and superficial femoral veins, the popliteal vein, tibioperoneal trunks, and posterior tibial and peroneal veins were examined, as well as gastrocnemius and soleus venous plexus and perforating veins. The main criterion for the diagnosis of DVT was the absence of a complete collapse of the vein when it was compressed transversally with the ultrasonographic probe; the absence of Doppler color flux allows an even more precise diagnosis. The aim of this study was not to evaluate the superficial venous system or the venous competence. We consider that 3 months is not time enough for the disappearance of an unnoticed venous thrombosis and even more so without anticoagulant treatment. All the examinations were performed by trained radiologists. The obesity status, still present only 3 months after the bariatric procedure, and the postsurgical changes make it difficult to perform a precise ultrasonographic evaluation of the porto-mesenteric axis; therefore a CT examination was elected. A Toshiba Aquilion device with 16 detector rows (Toshiba Medical Systems Corp.) was used. Iodine contrast was administered intravenously, and water was used as the oral contrast. Images were obtained in the portal phase. The absence of iodinated contrast in the superior mesenteric veins and/or portal vein was suggestive of thrombosed veins. The scoring of the mesenteric fat, the presence of edema or dilation of small bowel loops, liver perfusion defects, development of collateral veins, and even the presence of ascites were considered indirect signs of porto-mesenteric venous axis thrombosis. Variables

Analyzed variables were age, gender, comorbidities, complications, postoperative clinical history of DVT or PSMVT, and CT or Doppler US findings. Statistical analysis

All statistical analyses were performed using SPSS version 19.0 software (SPSS Inc., Chicago, IL). Gaussian distribution of the variables was analyzed using the Kolmogorov– Smirnoff test; P values >.05 were considered as Gaussian

DVT AND PSMVT AFTER LAPAROSCOPIC SLEEVE GASTRECTOMY

FIG. 1. Computed tomography scan shows thrombosis of the right branch of the portal vein. distribution. Quantitative variables following a normal distribution were defined by mean and standard deviation values; non-Gaussian variables were defined by median and range. Qualitative variables were defined by number of cases and percentages. The study was approved by the local Ethics Committee. All patients signed an informed consent form to be included in the study and to undergo the contrast-enhanced CT examination. Results

In total, 100 patients are included in the study (76 females and 24 males) with a mean age of 43.3 – 9.1 years. Comorbidities included hypertension in 32% of patients, type 2 diabetes mellitus in 28%, dyslipidemia in 50% (40% hypercholesterolemia and 10% hypertriglyceridemia), osteoarthritis in 24%, and obstructive sleep apnea hypopnea syndrome in 16%.

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Mean preoperative weight was 125.4 – 21.3 kg, and mean preoperative BMI was 49.9 – 7.2 kg/m2. Three months after surgery, mean weight was 95.2 – 15.8 kg, and mean BMI was 36.2 – 4.7 kg/m2, with a mean weight loss of 29.6 – 11 kg and mean excess BMI loss of 49.7 – 13.5%. Intraoperatively, there were no lacerations of portal or mesenteric vessels. Mean operative time was 115.4 – 21.3 minutes. Intra- or postoperative transfusions of packed red blood cells were necessary in only 4% of the patients. There were no cases of postoperative bleeding. Early postoperative complications appeared in 3 patients (3%): two staple line leaks and one intraabdominal abscess. Contrast-enhanced CT scan showed thrombosis of the porto-mesenteric axis in 1 case (1%). The patient was a 44-year-old male, with a clinical history of hypertension and type 2 diabetes mellitus and a preoperative weight of 142 kg and BMI of 48.2 kg/m2. The patient presented an uneventful postoperative course. The diagnosis was an incidental finding of thrombosis of the right branch of the portal vein during the CT scan performed 3 months after surgery (Fig. 1). At this time, the patient presented a weight of 111 kg, a BMI of 37.6 kg/m2, and an excess weight loss of 45.6%. Two patients presented DVT in the right leg. The first patient was a 32-year-old woman, without any relevant personal history, with a preoperative weight of 137.7 kg and BMI of 49.9 kg/m2. Three months after surgery, she presented a weight of 110.7 kg, BMI of 40.1 kg/m2, and excess weight loss of 39.5%. The DVT was clinically unnoticed. The second case of DVT was a 53-year-old woman, with a clinical history of dyslipidemia, type 2 diabetes mellitus, and sleep apnea hypopnea syndrome. Preoperative weight was 128 kg, and the corresponding BMI was 51.8 kg/m2. Three months after surgery she presented a weight of 107 kg, BMI of 43.3 kg/m2, and excess weight loss of 31.8%. Doppler US revealed an occupation with echogenic material that prevented the compression with the probe, and no Doppler flow could be evidenced (Fig. 2). Laboratory data did not show any relevant finding in the preoperative or in the 3-month postoperative determinations

FIG. 2. Doppler ultrasonography reveals an occupation with echogenic material that prevents the compression with the probe, and no Doppler flow could be evidenced.

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of the affected patients. Values for D dimers in these subjects were within the normal range. A subsequent hematology consultation failed to find hypercoagulability disorders in any of the patients. Anticoagulant treatment was started with enoxaparin (1 mg/kg/12 hours) during 3 days and later with acenocumarol during 6 months, adjusting the dosage to achieve an International Normalized Ratio between 2 and 3. The patients presented an uneventful course with evidence of complete resolution of the thrombus after finishing the treatment. Discussion

LSG is an emerging restrictive bariatric procedure, originally used as the first stage of other more complex techniques, but as a singular procedure, it has demonstrated excellent results in terms of weight lost and resolution of comorbidities, comparable to Roux-en-Y gastric bypass.13,15,16 Apart from the restrictive effect, LSG seems to present a certain hormonal effect, by reducing the segregation of ghrelin, an orexigenic hormone synthesized in the gastric fundus.15 The main complications of LSG are classified into intraoperative (splenic bleeding and bougie-related esophageal injury), early postoperative (staple line leak, abscess, fistula, bleeding, and wound complications), and delayed postoperative (port-site incisional hernias, mid-sleeve stricture, gastroesophageal reflux, and dilation of the gastric remnant, implying a weight regain) complication.1,5,14,17 Less frequent is PSMVT, which might extend to other tissues.3,5,7,17 In laparoscopic abdominal surgery, the increase of the intraabdominal pressure by the pneumperitoneum, the prolonged operation time, and the anti-Trendelenburg position are considered risk factors for PSMVT.5,6 It has been demonstrated that the splanchnic flow is inversely proportional to the pressure of the pneumoperitoneum. Moreover, the hypercapnia induces vasoconstriction. Obese patients require higher pneumoperitoneum pressures to obtain an adequate view. It has been also demonstrated that the surgical dissection induces the segregation of progoagulant cytokines.18 Other causes of PSMVT after bariatric surgery are the splenectomy as a surgical complication, the intraoperative portal vein lesion, and lack of vitamin K secondary to postoperative malabsorption.19,20 Clostridium difficile colitis,16,17 bacteremia caused by Bacteroides fragilis, and dehydration, especially after restrictive procedures, when patients hardly drink,21 are also considered to be risk factors for postoperative thrombotic events. Most PSMVT events after bariatric surgery present subacutely, occurring between postoperative Days 3 and 30. However, chronic PSMVT events are usually asymptomatic and unnoticed. Thus, they can develop into liver cirrhosis and its related complications.6,8,9 The incidence of DVT after laparoscopic bariatric surgery is around 3%, and that of pulmonary embolism is lower than 1%, but mortality after pulmonary embolism is estimated to be between 50% and 75%.6–9 Both PSMVT and DVT are life-threatening conditions. Several measures, including prophylactic LMWHs and compression stockings, are adopted to reduce their incidence. The problem is that there is no consensus about the optimal dosage of LMWHs. The dosage must be adjusted according to the weight of the patient, implying the need for administration of high preoperative doses. Intra- and postoperative

ALSINA ET AL.

bleeding is one of the main complications of bariatric surgery. Many surgeons fear these complications and administer lower doses of LMWH than the one recommended by most groups (0.5 mg/kg/day).14 On the other hand, some surgeons are more afraid of thrombosis than of bleeding and defend the administration of higher doses. Along the same line, the postoperative prolongation of the prophylaxis is also a debated issue, although most surgeons defend the maintenance of antithrombotic prophylaxis for 1 month, as laparoscopic bariatric surgery is considered a high-risk procedure performed in high-risk patients.14 One limitation of this study was the performance of both radiological tests postoperatively, but not preoperatively. Given that all the patients who presented thrombotic complications in the postoperative course were asymptomatic, we cannot completely discount the possible presence of these complications even before the bariatric surgery. Conclusions

The incidence of PSMVT and DVT after LSG with a prophylactic LMWH dose of 0.5 mg/kg/day and maintained for 30 days postoperatively is 1% and 2%, respectively. According to these results, a postoperative screening with Doppler US and/or contrast-enhanced CT seems to be unnecessary. Disclosure Statement

No competing financial interests exist. References

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Address correspondence to: Jaime Ruiz-Tovar, MD, PhD Department of Surgery General University Hospital Elche Camino de la Almazara, 11 03203–Elche, Alicante Spain E-mail: [email protected]

Incidence of deep vein thrombosis and thrombosis of the portal-mesenteric axis after laparoscopic sleeve gastrectomy.

Venous thromboembolism is the most common postoperative medical complication after bariatric surgery. Mortality associated with thromboembolic process...
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