Abstract
In recent years, both the actual number of overweight/obese individuals and their proportion of the population have steadily been rising worldwide and obesity‐related diseases have become major health concerns. In addition, as obesity is associated with an increased incidence of gastroenterological cancer, the number of obese patients has also been increasing in the field of gastroenterological surgery. While the influence of obesity on gastroenterological surgery has been widely studied, very few reports have focused on individual organs or surgical procedures, using a cross‐sectional study design. In the present review, we aimed to summarize the impacts of obesity on surgeries for the esophagus, stomach, colorectum, liver and pancreas. In general, obesity prolongs operative time. As to short‐term postoperative outcomes, obesity might be a risk for certain complications, depending on the procedure carried out. In contrast, it is possible that obesity doesn't adversely impact long‐term surgical outcomes. The influences of obesity on surgery are made even more complex by various categories of operative outcomes, surgical procedures, and differences in obesity among races. Therefore, it is important to appropriately evaluate perioperative risk factors, including obesity.
Keywords: body mass index, gastroenterological surgery, obesity, operative outcome
1. INTRODUCTION
The overweight/obese population has been steadily increasing worldwide. According to the WHO, with 1.3 billion overweight (25 < body mass index [BMI] < 30) people and 600 million obese (BMI > 30) people in the world,1 the obesity rate exceeds 10% for both genders and has more than doubled during the past 40 years.2 Furthermore, as seven of the top 10 causes of death/physical disability are chronic disorders such as cancer and diabetes, which are closely related to obesity,3 it can be said that obesity is among the world's major health concerns at present. According to “Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective” by the World Cancer Research Fund and American Cancer Society, gastroenterological cancer is known to be closely related to obesity as, in obese patients, the incidences of esophageal adenocarcinoma, colorectal cancer, and pancreatic cancer are clearly increased, while there is also a strong association with gallbladder cancer, and a possible association with liver cancer.4
In contrast, there are a number of reports describing the influences of obesity on gastroenterological surgery worldwide. However, the results are often difficult to pool because of differences among surgical procedures, surgical approaches, complications associated with specific organs/surgical methods, and obesity classifications. In addition, the events evaluated, such as short‐term outcomes (eg complications), long‐term outcomes (eg overall survival), and surgical outcomes (eg operative time, hemorrhage volume), often vary markedly among studies. The present review aims to provide an overview of how obesity affects gastroenterological surgery based on the recent literature. For this review, we organized recently reported surgical procedures according to anatomical/surgical techniques as the influences of obesity on surgery might differ among organs or surgical procedures.
2. GENERAL REMARKS: OBESITY PARADOX
Regarding gastroenterological cancer surgery, Shimada et al,5 conducting a systematic review, noted high BMI to be associated with postoperative morbidity rate, but not with poor oncological outcomes, whereas low BMI was significantly associated with inferior oncological outcomes. Mullen et al6 obtained similar results in a large‐scale review, showing the complication rate to be higher in obese than in normal weight patients, whereas 30‐day mortality was lower for overweight and obese patients than for those of normal weight, undergoing general surgeries other than vascular and bariatric operations (n = 118 707). According to the literature, BMI < 18.5 (underweight) is associated with particularly high rates of both complications and death.
As mentioned previously, the phenomenon wherein obesity provides an advantage against postoperative mortality is called the “Obesity paradox” and has been extensively described. In 2258 cases undergoing gastroenterological surgery (eg esophagectomy, gastrectomy, hepatectomy, pancreatectomy, low anterior resection (LAR)/proctectomy), morbidity was higher in those with BMI > 30, but mortality was still significantly better in this group than in the patients with normal BMI undergoing the same procedures.7 In contrast, mortality was higher in patients with BMI < 18.5 or BMI > 40.7 Benjamin et al8 indicated that both morbidity and mortality were more favorable in the obese than in the normal weight group receiving emergency abdominal surgery. A similar obesity paradox was indicated, by organ, for colorectal cancer surgery9, 10 and for gastric cancer surgery.11
This obesity paradox phenomenon has not, however, been confirmed for all surgical procedures in the field of gastroenterological surgery. A cross‐sectional analysis of the influences of obesity on surgery, examining multiple organs/surgical procedures, by our research group,12 indicated that operative time was prolonged as the BMI category rose for eight principal gastroenterological surgical procedures (n = 232 199) and mortality was also higher in patients with BMI > 30. Our prior study revealed that the overweight group tended to have the lowest mortality rate, an observation consistent with those made in cases undergoing colorectal cancer surgery/gastric cancer surgery. This was attributed to Asian populations having a higher percentage of body fat and a greater risk of obesity‐related comorbidities as compared to non‐Asians with similar BMI.13 By contrast, this phenomenon was not recognized in patients undergoing hepatectomy or pancreaticoduodenectomy (PD). In addition, Anazawa et al14 examined a risk model of 30‐day mortality for three gastroenterological surgery procedures (right hemicolectomy, LAR, PD) using a database from Japan and the USA. However, as mortality is significantly higher with LAR and PD for patients with BMI > 30 in Japan and the USA, respectively, the influences of obesity may vary not only among surgical procedures but also according to race.
3. ESOPHAGEAL CANCER SURGERY
The incidence of esophageal cancer is particularly high in the area from the east coast of the Caspian Sea to Northeast China via Central Asia, the so‐called Asian belt, and this cancer tends to be squamous cell carcinoma (SCC).15 In contrast, esophageal adenocarcinoma is frequently found in Western countries such as the UK/USA and the frequency has been increasing in recent years.16 Furthermore, the WHO concluded that the esophageal adenocarcinoma risk is clearly increased by obesity. As mentioned above, the characteristics of esophageal cancer differ markedly depending on histological features, allowing discrimination from other gastrointestinal malignant tumors. Thus, the influence of obesity on esophageal surgery should also be examined by focusing on histological type.
In examinations of the influences of obesity on esophageal surgery, the survival rate is often used as perioperative mortality is high compared to other gastrointestinal surgeries. As previously described in the systematic review by Shimada et al,5 it is often reported that outcomes are improved by high BMI and are, at least, not worsened by high BMI, according to meta‐analyses.17, 18, 19, 20 Furthermore, the influences of obesity on outcomes might reportedly differ depending on histological differences between adenocarcinoma or SCC.17, 21 In contrast, a number of studies focusing on the survival rate of underweight patients have demonstrated unfavorable outcomes.18, 22, 23 The reasons for obesity influencing outcomes may differ depending on whether BMI is high or low, in association with certain oncological background factors, such as tumor invasion which tends to be more aggressive in the underweight.18, 24 Table 1 shows a summary of past studies on the effects of obesity on outcomes of esophageal cancer surgery.
Table 1.
Year | Author | Country | n | BMI stratification | Operation | Disease | Outcome |
---|---|---|---|---|---|---|---|
2015 | Pan et al17 | China | 4823 |
<25, 25< or <24, 24< or 18.5‐25, 25< |
Eso | EC | High BMI is a potential predictor for better outcomes in EC patients overall, and particularly in EAC patients treated with curative esophagectomy. However, in ESCC patients, high BMI is a potential predictor of worse postoperative survival. |
2015 | Miao et al18 | China | 1342 | <18.5, 18.5‐25, 25< | ILE | EC | Incidence of pneumonia was higher in high BMI than in normal BMI subjects. However, chylothorax was less frequent in those with higher BMI. The better overall survival in high BMI compared with low BMI patients might be as a result of a relatively low pathological stage in the former. |
2013 | Zhang et al19 | China | 2031 | <18.5, 18.5‐23, 23< | Eso | EC | Patients with higher BMI had more postoperative complications, such as anastomotic leakage, but a lower incidence of chylothorax. They had a longer operative time than those of normal weight. High BMI was associated with significantly improved overall survival. |
2013 | Hong et al20 | China | 1988 | <25, 25‐30, 30< | Eso | EAC | Excess bodyweight did not predict the survival of patients with esophageal adenocarcinoma. |
2017 | Duan et al21 | China | 291 | 18.5‐23, 23‐27.5, 27.5< | Eso | ESCC | High BMI is a potential predictor of worse outcomes in ESCC patients. |
2016 | Kamachi et al22 | Japan | 340 | <18.5, 18.5< | Right TTE | ESCC | Overall survival and disease‐free survival rates were significantly lower in the BMI < 18.5 than in the BMI > 18.5 group. |
2015 | Hasegawa et al25 | Japan | 304 | <18.5, 18.5‐25, 25< | TTE | ESCC | On multivariate analysis, high BMI was a significant risk factor for anastomotic leakage. |
2012 | Blom et al26 | Netherlands | 736 | <25, 25‐30, 30< | TTE or THE | EC | Anastomotic leakage occurred more frequently in obese patients. |
BMI, body mass index; EAC, esophageal squamous cell carcinoma; EC, esophageal cancer; ESCC, esophageal squamous cell carcinoma; Eso, esophagectomy; ILE, Ivor‐Lewis esophagectomy; THE, transhiatal esophagectomy; TTE, transthoracic esophagectomy.
A high BMI may increase the risk of postoperative leakage, which is an important postoperative complication,24, 25, 26 but being underweight may increase the risk of postoperative chylothorax.18, 19 Many studies have demonstrated that operative times become increasingly prolonged as BMI increases.18, 19, 21, 24
4. GASTRIC CANCER SURGERY
East Asia is the source of several reviews on the influences of obesity on gastric cancer surgery, reflecting the high morbidity associated with this cancer in the region.15, 27
Chen et al11 reported an obesity paradox wherein overall survival was significantly better in patients with BMI > 25 than in those with normal BMI. Nonetheless, other than the aforementioned report, many studies failed to demonstrate any influence of obesity on long‐term survival.28, 29, 30, 31 By contrast, Struecker et al28 described short‐term survival (postoperative death) as being significantly poorer in patients with BMI > 30, whereas Kurita et al29 described survival as tending to be less favorable in those with BMI > 25. Obesity may have a negative influence on the short‐term survival of patients who have undergone gastrectomy.
The conclusion has often been reached, based on relatively large‐scale reports, that obesity negatively influences the postoperative complication rate. This negative influence might account for the high risks of complications such as incision infection, leakage, postoperative pneumonia, and intra‐abdominal abscess.30, 31, 32 In contrast, although BMI routinely serves as an obesity index, the visceral fat area (VFA) is reportedly a more appropriate predictor of complications.33, 34 Notably, VFA is often used as an obesity index for patients developing pancreatic fistula as a specific complication after gastrectomy, and an increase in VFA can serve as an important indicator of pancreatic fluid leakage risk.34, 35, 36
Reviews limited to laparoscopic surgery noted that obesity may prolong the operative time, without influencing either the complication rate or the survival rate.37, 38 These reviews suggest the safety and effectiveness of highly difficult laparoscopic surgery as compared to laparotomy. In addition, robotic surgery for gastric cancer has recently been conducted as a form of advanced medical care. Only a few studies have shown the superiority of robotic surgery in obese cases, but robotic surgery may not outperform laparoscopic surgery, in terms of complications. Furthermore, operative time is prolonged with robotic surgery as compared to laparoscopic surgery.39, 40 Table 2 shows a summary of past studies on the effects of obesity on outcomes of gastric cancer surgery.
Table 2.
Year | Author | Country | n | BMI stratification | Operation | Disease | Outcome |
---|---|---|---|---|---|---|---|
2015 | Chen et al11 | China | 1249 | <18.5, 18.5‐25, 25< | DG, TG, PG | GC | Despite a higher risk of postoperative complications, high BMI patients exhibited paradoxically superior overall survival as compared with normal BMI patients. Operative time was longer and blood loss was greater with higher BMI. |
2017 | Struecker et al28 | Germany | 249 | <30, 30< | Gastrectomy | GC | BMI > 30 was significantly associated with longer operative time, longer hospital stay, increased postoperative morbidity, and increased postoperative mortality. There was no significant difference in overall survival between the two groups. |
2015 | Kurita et al29 | Japan | 33 917 | <18.5, 18.5‐25, 25< | DG | GC | Operative mortality rate tended to be higher in the BMI > 25 than in the BMI < 25 group. |
2017 | Kikuchi et al30 | Japan | 39 253 | <25, 25‐30, 30‐35, 35< | TG | GC | BMI > 25 was identified as a risk factor for SSI, pancreatic fistula, pneumonia, prolonged ventilation over 48 h, and renal failure. |
2013 | Bickenbach et al31 | USA | 1853 | <25, 25< | Gastrectomy | GC | Higher BMI was associated with increased rates of wound infection and anastomotic leakage. There was no difference in overall survival or disease‐specific survival between the two groups. |
2017 | Kunisaki et al32 | Japan | 65 906 |
<25, 25< or <30, 30< |
DG | GC | BMI > 25 was a risk factor predicting pneumonia and anastomotic leakage, while BMI > 30 was a risk factor for unplanned intubation, renal failure and blood transfusion >5 units. |
2012 | Sugisawa et al34 | Japan | 206 | VFA | DG, TG | GC | VFA was found to be an independent risk factor for both pancreas‐related infection and anastomotic leakage. |
2014 | Jung et al38 | Korea | 1512 | <25, 25‐30, 30< | LDG | GC | BMI > 30 patients had a significantly longer operative time than those with normal BMI, but there were no significant differences in either intraoperative blood loss or other complications between the two groups. Postoperative morbidity and mortality rates in the BMI > 30 group did not differ significantly from those of the normal BMI group. |
2016 | Park et al39 | Korea | 434 | <25, 25< | RG, LG | GC | Operative time was significantly longer in patients with BMI > 25 than in those with BMI < 25. Estimated blood loss, complication rates, open conversion rate, and length of hospital stay did not differ between the obese robotic and obese laparoscopic groups. |
BMI, body mass index; DG, distal gastrectomy; GC, gastric cancer; LADG, laparoscopy‐assisted distal gastrectomy; LDG, laparoscopic distal gastrectomy; LG, laparoscopic gastrectomy; PG, proximal gastrectomy; RG, robotic gastrectomy; SSI, surgical site infection; TG, total gastrectomy; VFA, visceral fat area.
5. COLORECTAL SURGERY
More reviews of the impact of obesity on surgery have focused on the colon than any other organ. From an oncological viewpoint, obesity is widely regarded as being related to the morbidity of colorectal cancer.
As described previously, postoperative morbidity appears to be increased by obesity in patients undergoing colon surgery. However, the obesity paradox phenomenon is reflected by the mildly obese having the lowest operative mortality, whereas the highest operative mortality is associated with extreme obesity.9, 10 Similarly, Hussan et al41 and Matsubara et al42 reported that BMI > 40 in patients undergoing colorectal cancer surgery and BMI > 30 in those receiving LAR are independently associated with higher operative mortality. The difference in BMI categories is regarded as a difference in body fat percentage between races, as noted above.13 The review by Shimada et al5 describes a low BMI as correlating with reduced survival for underweight patients.
There are other studies demonstrating obesity to have a negative influence on complications. Several studies have identified a high risk of surgical site infection (SSI) with obesity.43, 44 Similar adverse influences have been recognized for surgical procedures such as right hemicolectomy,45 LAR,46, 47 Hartmann surgery,48 Miles surgery,49 and robotic surgery.50 Moreover, obesity might reportedly be an independent risk factor for leakage.51, 52
A meta‐analysis (n = 4550) of laparoscopic surgery by Fung et al53 found that, for colorectal cancer surgery, SSI, leakage, morbidity, and conversion rate are significantly higher in patients with BMI > 30 than in those with normal BMI. Table 3 shows a summary of past studies on the effects of obesity on outcomes of colorectal surgery. Although some studies have not found obesity to influence all of these complications, the association of obesity with prolonged operative time has consistently been recognized.54, 55 Obesity reportedly does not influence intraoperative variables or postoperative complications in patients with inflammatory bowel diseases, such as Crohn's disease and ulcerative colitis, undergoing gastrointestinal surgical resection.56
Table 3.
Year | Author | Country | n | BMI stratification | Operation | Disease | Outcome |
---|---|---|---|---|---|---|---|
2016 | Alizadeh et al9 | USA | 206 360 | <18.5, 18.5‐25, 25‐30, 30‐40, 40< | Colectomy with rectal resection | Various | Obesity (30 < BMI < 40) was associated with a higher overall morbidity rate and lower in‐hospital mortality rate than normal BMI. Morbidly obese (BMI > 40) subjects had higher overall morbidity and in‐hospital mortality rates than those with normal BMI. |
2016 | Govaert et al10 | Netherlands | 8687 | 18.5‐25, 25‐30, 30‐35, 35< | Colectomy with rectal resection | CRC | BMI > 30 was associated with more complications, prolonged operative times and longer hospital stays. Mortality rates were significantly lower in the 25 < BMI < 30 group and significantly higher in the BMI > 35 group than in those with normal BMI. |
2016 | Hussan et al41 | USA | 85 300 | <30, 40< | Colectomy with rectal resection | CRC | Morbid obesity (BMI > 40) was associated with an increased perioperative mortality rate and more surgical complications. |
2014 | Matsubara et al42 | Japan | 16 695 | <30, 30< | LAR | RC | Risk model showed BMI > 30 to be an independent risk factor for both 30‐day and operative mortality. |
2016 | Wilson et al43 | USA | 47 868 | <20, 21‐25, 26‐30, 30< | Colectomy | Various | Obesity was associated with a higher risk of superficial and deep SSI. |
2017 | Watanabe et al46 | Japan | 33 411 | <26, 26< | LAR | RC | Obesity increased the risk for operative site infection but not for either leakage or renal failure. |
2016 | Althumairi et al49 | USA | 8449 | 18.5<, 18.5‐25, 25‐35, 35< | APR | RC | BMI > 35 was a risk factor for deep SSI and wound dehiscence. |
2017 | Nikolian et al51 | USA | 9192 | <30, 30< | Colectomy with rectal resection | Various | Multivariable analysis showed BMI > 30 to be independently associated with anastomotic leakage. |
2015 | Frasson et al52 | Spain | 3193 | <30, 30< | Colectomy | CC | Obesity was shown to be an independent risk factor for anastomotic leakage on multivariate analysis. |
2017 | Fung et al53 | Canada | 4550 | <30, 30< | Laparoscopic colectomy with rectal resection | CRC | Overall survival and disease‐free survival were similar in the two groups. The conversion rate, postoperative morbidity, wound infection and anastomotic leakage were all significantly increased in the obese group. |
APR, abdominoperineal resection; BMI, body mass index; CC, colon cancer; CRC, colorectal cancer; LAR, low anterior resection; RC, rectal cancer; SSI, surgical site infection.
6. LIVER SURGERY
There are fewer large‐scale reviews focusing on the influences of obesity on liver surgery than on gastrointestinal surgery. The main diseases studied are hepatocellular carcinoma and liver metastasis of colorectal cancer, but there are reviews actually targeting all hepatic disorders.57, 58, 59, 60, 61, 62, 63, 64, 65, 66, 67 Table 4 shows a summary of past studies on the effects of obesity on outcomes of liver surgery. Our group conducted a large‐scale review to examine the impacts of obesity on hepatic resection and found that obesity (BMI > 30) prolonged operative time by approximately 50 min as compared to surgery on non‐obese patients undergoing hepatectomy of more than one segment apart from the lateral segment (n = 14 903).12 In addition, Yokoo et al57, studying a similar surgical group, reported BMI > 30 to potentially be a risk factor for blood transfusion and BMI > 35 to be a risk factor for unplanned intubation (n = 14 970). In a similar report, Langella et al58 noted that resection time, blood loss, and rate of pulmonary complications tended to rise if BMI > 30, and that obesity may negatively influence all three of these factors. In another large‐scale review, Mathur et al59 found that obese patients had significantly higher odds of having a complication than normal‐weight patients (n=3960). However, because obesity may reportedly not influence postoperative complications in some cases, it is hoped that such cases can be analyzed in a future meta‐analysis.60, 61, 62, 63
Table 4.
Year | Author | Country | n | BMI stratification | Operation | Disease | Outcome |
---|---|---|---|---|---|---|---|
2016 | Yokoo et al57 | Japan | 14 970 |
<30, 30< or <35, 35< |
Hx | Various | BMI > 30 was a risk factor for blood transfusion >5 units and renal failure, while BMI > 35 was a risk factor for unplanned intubation and cardiac events, according to a risk model for morbidities. |
2015 | Langella et al58 | Italy | 1021 | <30, 30< | Hepatectomy | Colorectal metastasis | Transection time and blood loss were greater in BMI > 30 subjects. There was no difference in postoperative mortality between the two groups. Overall morbidity was greater in BMI > 30 subjects, mainly as a result of pulmonary complications. On multivariate analysis, obesity independently predicted overall morbidity. |
2010 | Mathur et al59 | USA | 3960 | 18.5<, 18.5‐25, 25‐30, 30< | Hepatectomy | Various | Compared to normal‐weight patients, obese patients had significantly higher odds of having a complication. Obesity was not a significant predictor of mortality. |
2015 | Nomi et al61 | France | 228 | <25, 25‐30, 30< | Laparoscopic hepatectomy | Various | There were no significant differences in rates of postoperative mortality and overall complications. |
2014 | Wang et al63 | China | 1543 | <18.5, 18.5‐24, 24‐28, 28< | Hepatectomy | HBV‐related HCC | Mortality and total complications differed minimally among the four groups except for underweight patients having fewer total complications. Postoperative wound complications were more common in overweight and obese patients. |
2014 | Kenjo et al64 | Japan | 7732 | <30, 30< | Hx | Various | There were no differences in either the 30‐day mortality rate or the 90‐day in‐hospital mortality rate between obese and non‐obese patients. |
2015 | Saab et al65 | USA | 74 487 | Various | Liver transplantation | Various | Obesity did not adversely impact patient survival. |
2015 | Conzen et al67 | USA | 785 | <18, 18‐25, 25‐30, 30‐35, 35‐40, 40< | Liver transplantation | Various | Cox regression analysis confirmed BMI > 40 to be an independent predictor of poor survival. |
BMI, body mass index; HBV, hepatitis B virus; HCC, hepatocellular carcinoma; Hx, hepatectomy of more than one segment other than the lateral segment.
Examining the influence of obesity on mortality, Kenjo et al64 concluded that obesity (BMI > 30) had no influence on either the 30‐day mortality rate or on the 90‐day in‐hospital mortality rate, based on developing a risk model for mortality in patients who had received hepatectomy (n = 7732). Similar results were obtained by several other investigators.58, 61, 62, 63 Based on the aforementioned results, even in hepatectomy, obesity was considered to be associated with certain complications but did not worsen survival according to the systematic review conducted by Shimada et al5.
As to the influence of obesity on liver transplantation recipients, Saab et al65 conducted a meta‐analysis (n = 74 487) showing that BMI does not influence either mortality or survival. However, obese patients had poorer survival in subgroup analyses of studies whose cohorts of obese and non‐obese patients had similar causes of liver disease.65 Furthermore, some studies have found that extreme obesity may increase mortality and worsen survival.66, 67
7. PANCREATIC SURGERY
In pancreatectomy including various procedures, obesity was defined as a risk factor for the occurrence of postoperative complications.68, 69 Notably, several investigations have focused on pancreatic fistula after pancreatectomy, which is among the specific complications experienced. Ramsey and Martin70 described pooled analyses, conducted as part of a meta‐analysis, as showing a significant association between pancreatic fistula and BMI (n = 2736). Given these observations, increased BMI, which correlates with soft pancreatic consistency, a known risk factor for pancreatic fistula, might be among its causes.71, 72 Obesity is frequently reported to exert no influence on operative mortality in patients with pancreatic malignancies, as is the case with surgeries on other organs.68, 69, 70
In pancreaticoduodenectomy, numerous reviews have also consistently described obesity as exerting a negative influence.73, 74, 75, 76, 77 Aoki et al73, applying a risk model (n = 17 564), suggested BMI > 25 to potentially be a factor predicting severe complications (Clavien Dindo Classification Grade 4 or higher) including pancreatic fistula (International Study Group Pancreatic Fistula Grade C). In addition, obesity has been identified as a risk factor for severe complications74, 75 but not operative mortality.76, 77 As with hepatectomy, obesity was found to be associated with increased intraoperative blood loss.69, 75 Even with other surgical procedures, such as distal pancreatectomy and central pancreatectomy, obesity was also identified as a risk factor for complications.78, 79 Table 5 shows a summary of past studies on the effects of obesity on outcomes of pancreatic surgery.
Table 5.
Year | Author | Country | n | BMI stratification | Operation | Disease | Outcome |
---|---|---|---|---|---|---|---|
2015 | Chen et al68 | China | 362 | <24, 24< | Pancreatectomy | Various | Higher BMI increased the risk for postoperative complications. There were no significant differences in mortality rates. |
2017 | Aoki et al73 | Italy | 17 564 | <25, 25< | PD | Various | Obesity was a significant risk factor for pancreatic fistula with an International Study Group of Pancreatic Fistula (ISGPF) grade C and for severe morbidity. |
2016 | Wiltberger et al74 | Germany | 405 | <25, 25‐30, 30< | PPPD | Various | On multivariate analysis, obesity was a significant predictor of major complications. |
2014 | El Nakeeb et al75 | Egypt | 471 | <25, 25< | PD | Various | Operative time was significantly longer in overweight patients. Overall complication, pancreatic fistula and hospital mortality rates were significantly higher in overweight patients. |
2016 | Pecorelli et al76 | Italy | 202 | VFA | PPPD | Malignancy | VFA was an independent predictor of pancreatic fistula and was associated with the 60‐day postoperative mortality rate. |
2011 | Greenblatt et al77 | USA | 4945 | <18, 18‐25, 25‐30, 30‐35, 35‐40, 40< | PD or PPPD | Various | BMI > 25 was a significant predictor of morbidity, but not of 30‐day mortality. |
2016 | Sahakyan et al78 | Norway | 423 | 18‐25, 25‐30, 30< | Lap DP | Various | Patients with BMI > 30 had significantly longer operative times and increased blood loss as compared with the other groups. Postoperative complication and pancreatic fistula rates were significantly higher in the BMI > 30 than in the normal BMI group. |
2012 | Dumitrascu et al79 | Romania | 24 | <30, 30< | CP | Various | On multivariate analysis, BMI > 30 correlated significantly with the development of complications. |
BMI, body mass index; CP, central pancreatectomy; Lap DP, laparoscopic distal pancreatectomy; PD, pancreaticoduodenectomy; PPPD, pylorus‐preserving pancreaticoduodenectomy; VFA, visceral fat area.
Pecorelli et al76 reported VFA to be an independent risk factor for pancreatic fistula, similar to its influence as a risk factor for pancreatic fistula after gastrectomy. This suggests VFA to possibly be a more precise indicator than BMI in patients undergoing pancreatectomy because increased VFA may exert a direct effect making surgical techniques more complicated. In addition, Pecorelli et al76 addressed the combination of visceral obesity and sarcopenia as the best predictor of postoperative death.
8. CONCLUSIONS
Obesity is generally considered to exert an adverse effect on major gastroenterological surgeries. In particular, obesity prolongs operative time and may thus be a risk factor for short‐term complications. However, obesity may not adversely influence long‐term surgical outcomes. The influences of obesity on surgery may vary depending on the surgical procedure, surgical outcome and/or racial differences in obesity. Preoperative assessment with consideration of not only obesity but also other operative risks is essential for all surgical procedures.
DISCLOSURE
Authors declare no conflicts of interest for this article.
Ri M, Aikou S, Seto Y. Obesity as a surgical risk factor. Ann Gastroenterol Surg. 2018;2:13–21. https://doi.org/10.1002/ags3.12049
REFERENCES
- 1. WHO . Obesity and overweight. Fact sheet N°311. Geneva: World Health Organization; 2015. [Google Scholar]
- 2. NCD Risk Factor Collaboration (NCD‐RisC) . Trends in adult body‐mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population‐based measurement studies with 19·2 million participants. Lancet. 2016;387:1377–96. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3. National Center for Health Statistics (US) . Health, United States, 2015: With special feature on racial and ethnic health disparities. Hyattsville, MD: National Center for Health Statistics, 2016: 461. [PubMed] [Google Scholar]
- 4. World Cancer Research Fund/American Institute for Cancer Research . Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Washington DC: AICR; 2007. [Google Scholar]
- 5. Shimada H, Fukunaga T, Haga Y. Does postoperative morbidity worsen the oncological outcome after radical surgery for gastrointestinal cancers? A systematic review of the literature. Ann Gastroenterol Surg. 2017;1:11–23. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. Mullen JT, Moorman DW, Davenport DL. The obesity paradox: body mass index and outcomes in patients undergoing nonbariatric general surgery. Ann Surg. 2009;250:166–72. [DOI] [PubMed] [Google Scholar]
- 7. Mullen JT, Davenport DL, Hutter MM, et al. Impact of body mass index on perioperative outcomes in patients undergoing major intra‐abdominal cancer surgery. Ann Surg Oncol. 2008;15:2164–72. [DOI] [PubMed] [Google Scholar]
- 8. Benjamin ER, Dilektasli E, Haltmeier T, Beale E, Inaba K, Demetriades D. The effects of body mass index on complications and mortality after emergency abdominal operations: the obesity paradox. Am J Surg. 2017. [Epub ahead of print]. https://doi.org/10.1016/j.amjsurg.2017.01.023. [DOI] [PubMed] [Google Scholar]
- 9. Alizadeh RF, Moghadamyeghaneh Z, Whealon MD, et al. Body mass index significantly impacts outcomes of colorectal surgery. Am Surg. 2016;82:930–5. [PubMed] [Google Scholar]
- 10. Govaert JA, Lijftogt N, van Dijk WA, et al. Colorectal cancer surgery for obese patients: financial and clinical outcomes of a Dutch population‐based registry. J Surg Oncol. 2016;113:489–95. [DOI] [PubMed] [Google Scholar]
- 11. Chen HN, Chen XZ, Zhang WH, et al. The Impact of body mass index on the surgical outcomes of patients with gastric cancer: a 10‐year, single‐institution cohort study. Medicine (Baltimore). 2015;94:e1769. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Ri M, Miyata H, Aikou S, et al. Effects of body mass index (BMI) on surgical outcomes: a nationwide survey using a Japanese web‐based database. Surg Today. 2015;45:1271–9. [DOI] [PubMed] [Google Scholar]
- 13. Wen CP, David Cheng TY, Tsai SP, et al. Are Asians at greater mortality risks for being overweight than Caucasians? Redefining obesity for Asians. Public Health Nutr. 2009;12:497–506. [DOI] [PubMed] [Google Scholar]
- 14. Anazawa T, Paruch JL, Miyata H, et al. Comparison of national operative mortality in gastroenterological surgery using web‐based prospective data entry systems. Medicine (Baltimore). 2015;94:e2194. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet‐Tieulent J, Jemal A. Global cancer statistics, 2012. A Cancer J Clin. 2015;65:87–108. [DOI] [PubMed] [Google Scholar]
- 16. Pohl H, Welch HG. The role of overdiagnosis and reclassification in the marked increase of esophageal adenocarcinoma incidence. J Natl Cancer Inst. 2005. Jan;97:142–6. [DOI] [PubMed] [Google Scholar]
- 17. Pan W, Sun Z, Xiang Y, Fang W. The correlation between high body mass index and survival in patients with esophageal cancer after curative esophagectomy: evidence from retrospective studies. Asia Pac J Clin Nutr. 2015;24:480–8. [DOI] [PubMed] [Google Scholar]
- 18. Miao L, Chen H, Xiang J, Zhang Y. A high body mass index in esophageal cancer patients is not associated with adverse outcomes following esophagectomy. J Cancer Res Clin Oncol. 2015;141:941–50. [DOI] [PubMed] [Google Scholar]
- 19. Zhang SS, Yang H, Luo KJ, et al. The impact of body mass index on complication and survival in resected oesophageal cancer: a clinical‐based cohort and meta‐analysis. Br J Cancer. 2013;109:2894–903. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20. Hong L, Zhang H, Zhao Q, Han Y, Yang J, Brain L. Relation of excess body weight and survival in patients with esophageal adenocarcinoma: a meta‐analysis. Dis Esophagus. 2013;26:623–7. [DOI] [PubMed] [Google Scholar]
- 21. Duan XF, Tang P, Shang XB, Jiang HJ, Zhao Q, Yu ZT. High body mass index worsens survival in patients with esophageal squamous cell carcinoma after esophagectomy. Dig Surg. 2017;34:319–27. [DOI] [PubMed] [Google Scholar]
- 22. Kamachi K, Ozawa S, Hayashi T, Kazuno A, Ito E, Makuuchi H. Impact of body mass index on postoperative complications and long‐term survival in patients with esophageal squamous cell cancer. Dis Esophagus. 2016;29:229–35. [DOI] [PubMed] [Google Scholar]
- 23. Wang F, Duan H, Cai M, et al. Prognostic significance of the pN classification supplemented by body mass index for esophageal squamous cell carcinoma. Thorac Cancer. 2015;6:765–71. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24. Grotenhuis BA, Wijnhoven BP, Hötte GJ, van der Stok EP, Tilanus HW, van Lanschot JJ. Prognostic value of body mass index on short‐term and long‐term outcome after resection of esophageal cancer. World J Surg. 2010;34:2621–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25. Hasegawa T, Kubo N, Ohira M, et al. Impact of body mass index on surgical outcomes after esophagectomy for patients with esophageal squamous cell carcinoma. J Gastrointest Surg. 2015;19:226–33. [DOI] [PubMed] [Google Scholar]
- 26. Blom RL, Lagarde SM, Klinkenbijl JH, Busch OR, van Berge Henegouwen MI. A high body mass index in esophageal cancer patients does not influence postoperative outcome or long‐term survival. Ann Surg Oncol. 2012;19:766–71. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27. Wu CY, Lin JT. The changing epidemiology of Asian digestive cancers: from etiologies and incidences to preventive strategies. Best Pract Res Clin Gastroenterol. 2015;29:843–53. [DOI] [PubMed] [Google Scholar]
- 28. Struecker B, Biebl M, Dadras M, et al. The impact of obesity on outcomes following resection for gastric cancer. Dig Surg. 2017;34:133–41. [DOI] [PubMed] [Google Scholar]
- 29. Kurita N, Miyata H, Gotoh M, et al. Risk model for distal gastrectomy when treating gastric cancer on the basis of data from 33,917 Japanese patients collected using a nationwide web‐based data entry system. Ann Surg. 2015;262:295–303. [DOI] [PubMed] [Google Scholar]
- 30. Kikuchi H, Miyata H, Konno H, et al. Development and external validation of preoperative risk models for operative morbidities after total gastrectomy using a Japanese web‐based nationwide registry. Gastric Cancer. 2017. [Epub ahead of print]. https://doi.org/10.1007/s10120‐017‐0706‐9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31. Bickenbach KA, Denton B, Gonen M, Brennan MF, Coit DG, Strong VE. Impact of obesity on perioperative complications and long‐term survival of patients with gastric cancer. Ann Surg Oncol. 2013;20:780–7. [DOI] [PubMed] [Google Scholar]
- 32. Kunisaki C, Miyata H, Konno H, et al. Modeling preoperative risk factors for potentially lethal morbidities using a nationwide Japanese web‐based database of patients undergoing distal gastrectomy for gastric cancer. Gastric Cancer. 2017;20:496–507. [DOI] [PubMed] [Google Scholar]
- 33. Takeuchi M, Ishii K, Seki H, et al. Excessive visceral fat area as a risk factor for early postoperative complications of total gastrectomy for gastric cancer: a retrospective cohort study. BMC Surg. 2016;16:54. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34. Sugisawa N, Tokunaga M, Tanizawa Y, Bando E, Kawamura T, Terashima M. Intra‐abdominal infectious complications following gastrectomy in patients with excessive visceral fat. Gastric Cancer. 2012;15:206–12. [DOI] [PubMed] [Google Scholar]
- 35. Sato Y, Inokuchi M, Otsuki S, Fujimori Y, Kojima K. Risk factor of pancreatic fistula after radical gastrectomy from the viewpoint of fatty pancreas. Dig Surg. 2017. [Epub ahead of print]. https://doi.org/10.1159/000455332. [DOI] [PubMed] [Google Scholar]
- 36. Tanaka K, Miyashiro I, Yano M, et al. Accumulation of excess visceral fat is a risk factor for pancreatic fistula formation after total gastrectomy. Ann Surg Oncol. 2009;16:1520–5. [DOI] [PubMed] [Google Scholar]
- 37. Wang Z, Zhang X, Liang J, Hu J, Zeng W, Zhou Z. Short‐term outcomes for laparoscopy‐assisted distal gastrectomy for body mass index ≥30 patients with gastric cancer. J Surg Res. 2015;195:83–8. [DOI] [PubMed] [Google Scholar]
- 38. Jung JH, Ryu SY, Jung MR, Park YK, Jeong O. Laparoscopic distal gastrectomy for gastric cancer in morbidly obese patients in South Korea. J Gastric Cancer. 2014;14:187–95. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39. Park JM, Kim HI, Han SU, et al. Who may benefit from robotic gastrectomy?: a subgroup analysis of multicenter prospective comparative study data on robotic versus laparoscopic gastrectomy. Eur J Surg Oncol. 2016;42:1944–9. [DOI] [PubMed] [Google Scholar]
- 40. Park JY, Ryu KW, Reim D, et al. Robot‐assisted gastrectomy for early gastric cancer: is it beneficial in viscerally obese patients compared to laparoscopic gastrectomy? World J Surg. 2015;39:1789–97. [DOI] [PubMed] [Google Scholar]
- 41. Hussan H, Gray DM, Hinton A, Krishna SG, Conwell DL, Stanich PP. Morbid obesity is associated with increased mortality, surgical complications, and incremental health care utilization in the peri‐operative period of colorectal cancer surgery. World J Surg. 2016;40:987–94. [DOI] [PubMed] [Google Scholar]
- 42. Matsubara N, Miyata H, Gotoh M, et al. Mortality after common rectal surgery in Japan: a study on low anterior resection from a newly established nationwide large‐scale clinical database. Dis Colon Rectum. 2014;57:1075–81. [DOI] [PubMed] [Google Scholar]
- 43. Wilson MZ, Dillon PW, Stewart DB, Hollenbeak CS. Timing of postoperative infections after colectomy: evidence from NSQIP. Am J Surg. 2016;212:844–50. [DOI] [PubMed] [Google Scholar]
- 44. Tserenpuntsag B, Haley V, Van Antwerpen C, et al. Surgical site infection risk factors identified for patients undergoing colon procedures, New York State 2009‐2010. Infect Control Hosp Epidemiol. 2014;35:1006–12. [DOI] [PubMed] [Google Scholar]
- 45. Frasson M, Granero‐Castro P, Ramos Rodríguez JL, et al. Risk factors for anastomotic leak and postoperative morbidity and mortality after elective right colectomy for cancer: results from a prospective, multicentric study of 1102 patients. Int J Colorectal Dis. 2016;31:105–14. [DOI] [PubMed] [Google Scholar]
- 46. Watanabe T, Miyata H, Konno H, et al. Prediction model for complications after low anterior resection based on data from 33,411 Japanese patients included in the National Clinical Database. Surgery. 2017;161:1597–608. [DOI] [PubMed] [Google Scholar]
- 47. Hrabe JE, Sherman SK, Charlton ME, Cromwell JW, Byrn JC. Effect of BMI on outcomes in proctectomy. Dis Colon Rectum. 2014;57:608–15. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48. Brathwaite S, Latchana N, Esemuede I, Harzman A, Husain S. Risk factors for surgical site infection in open and laparoscopic Hartmann closure: a multivariate analysis. Surg Laparosc Endosc Percutan Tech. 2017;27:51–3. [DOI] [PubMed] [Google Scholar]
- 49. Althumairi AA, Canner JK, Gearhart SL, et al. Risk factors for wound complications after abdominoperineal excision: analysis of the ACS NSQIP database. Colorectal Dis. 2016;18:O260–6. [DOI] [PubMed] [Google Scholar]
- 50. Harr JN, Luka S, Kankaria A, Juo YY, Agarwal S, Obias V. Robotic‐assisted colorectal surgery in obese patients: a case‐matched series. Surg Endosc. 2017;31:2813–9. [DOI] [PubMed] [Google Scholar]
- 51. Nikolian VC, Kamdar NS, Regenbogen SE, et al. Anastomotic leak after colorectal resection: a population‐based study of risk factors and hospital variation. Surgery. 2017;161:1619–27. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52. Frasson M, Flor‐Lorente B, Rodríguez JL, et al. Risk factors for anastomotic leak after colon resection for cancer: multivariate analysis and nomogram from a multicentric, prospective, national study with 3193 patients. Ann Surg. 2015;262:321–30. [DOI] [PubMed] [Google Scholar]
- 53. Fung A, Trabulsi N, Morris M, et al. Laparoscopic colorectal cancer resections in the obese: a systematic review. Surg Endosc. 2017;31:2072–88. [DOI] [PubMed] [Google Scholar]
- 54. Xia X, Huang C, Jiang T, et al. Is laparoscopic colorectal cancer surgery associated with an increased risk in obese patients? A retrospective study from China. World J Surg Oncol. 2014;12:184. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55. Miyamoto Y, Ishii T, Tashiro J, et al. Effects of obesity on the outcome of laparoscopic surgery for colorectal cancer. Surg Today. 2014;44:1293–9. [DOI] [PubMed] [Google Scholar]
- 56. Guardado J, Carchman E, Danicic AE, et al. Obesity does not impact perioperative or postoperative outcomes in patients with inflammatory bowel disease. J Gastrointest Surg. 2016;20:725–33. [DOI] [PubMed] [Google Scholar]
- 57. Yokoo H, Miyata H, Konno H, et al. Models predicting the risks of six life‐threatening morbidities and bile leakage in 14,970 hepatectomy patients registered in the National Clinical Database of Japan. Medicine (Baltimore). 2016;95:e5466. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 58. Langella S, Russolillo N, Forchino F, Lo Tesoriere R, D'Eletto M, Ferrero A. Impact of obesity on postoperative outcome of hepatic resection for colorectal metastases. Surgery. 2015;158:1521–9. [DOI] [PubMed] [Google Scholar]
- 59. Mathur AK, Ghaferi AA, Osborne NH, et al. Body mass index and adverse perioperative outcomes following hepatic resection. J Gastrointest Surg. 2010;14:1285–91. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 60. Uchida H, Iwashita Y, Saga K, et al. Benefit of laparoscopic liver resection in high body mass index patients. World J Gastroenterol. 2016;22:3015–22. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61. Nomi T, Fuks D, Ferraz JM, Kawaguchi Y, Nakajima Y, Gayet B. Influence of body mass index on postoperative outcomes after laparoscopic liver resection. Surg Endosc. 2015;29:3647–54. [DOI] [PubMed] [Google Scholar]
- 62. Guo Z, Zhang J, Jiang JH, Li LQ, Xiang BD. Obesity does not influence outcomes in hepatocellular carcinoma patients following curative hepatectomy. PLoS ONE. 2015;10:e0125649. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 63. Wang H, Yang J, Zhang X, Yan L, Yang J. Liver resection in hepatitis B‐related hepatocellular carcinoma: clinical outcomes and safety in overweight and obese patients. PLoS ONE. 2014;9:e99281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64. Kenjo A, Miyata H, Gotoh M, et al. Risk stratification of 7,732 hepatectomy cases in 2011 from the National Clinical Database for Japan. J Am Coll Surg. 2014;218:412–22. [DOI] [PubMed] [Google Scholar]
- 65. Saab S, Lalezari D, Pruthi P, Alper T, Tong MJ. The impact of obesity on patient survival in liver transplant recipients: a meta‐analysis. Liver Int. 2015;35:164–70. [DOI] [PubMed] [Google Scholar]
- 66. Molina Raya A, García Navarro A, San Miguel Méndez C, et al. Influence of obesity on liver transplantation outcomes. Transplant Proc. 2016;48:2503–5. [DOI] [PubMed] [Google Scholar]
- 67. Conzen KD, Vachharajani N, Collins KM, et al. Morbid obesity in liver transplant recipients adversely affects longterm graft and patient survival in a single‐institution analysis. HPB (Oxford). 2015;17:251–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 68. Chen YT, Deng Q, Che X, et al. Impact of body mass index on complications following pancreatectomy: ten‐year experience at National Cancer Center in China. World J Gastroenterol. 2015;21:7218–24. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 69. Benns M, Woodall C, Scoggins C, McMasters K, Martin R. The impact of obesity on outcomes following pancreatectomy for malignancy. Ann Surg Oncol. 2009;16:2565–9. [DOI] [PubMed] [Google Scholar]
- 70. Ramsey AM, Martin RC. Body mass index and outcomes from pancreatic resection: a review and meta‐analysis. J Gastrointest Surg. 2011;15:1633–42. [DOI] [PubMed] [Google Scholar]
- 71. Mathur A, Pitt HA, Marine M, et al. Fatty pancreas: a factor in postoperative pancreatic fistula. Ann Surg. 2007;246:1058–64. [DOI] [PubMed] [Google Scholar]
- 72. Callery MP, Pratt WB, Ken TS, Chaikof EL, Vollmer CM. A prospectively validated clinical risk score accurately predicts pancreatic fistula after pancreaticoduodenectomy. J Am Coll Surg. 2013;216:1–14. [DOI] [PubMed] [Google Scholar]
- 73. Aoki S, Miyata H, Gotoh M, et al. Risk factors of serious postoperative complications after pancreaticoduodenectomy and risk calculators for predicting postoperative complications: a nationwide study of 17,564 patients in Japan. J Hepatobiliary Pancreat Sci. 2017;24:243–51. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 74. Wiltberger G, Muhl B, Benzing C, et al. Preoperative risk stratification for major complications following pancreaticoduodenectomy: identification of high‐risk patients. Int J Surg. 2016;31:33–9. [DOI] [PubMed] [Google Scholar]
- 75. El Nakeeb A, Hamed H, Shehta A, et al. Impact of obesity on surgical outcomes post‐pancreaticoduodenectomy: a case‐control study. Int J Surg. 2014;12:488–93. [DOI] [PubMed] [Google Scholar]
- 76. Pecorelli N, Carrara G, De Cobelli F, et al. Effect of sarcopenia and visceral obesity on mortality and pancreatic fistula following pancreatic cancer surgery. Br J Surg. 2016;103:434–42. [DOI] [PubMed] [Google Scholar]
- 77. Greenblatt DY, Kelly KJ, Rajamanickam V, et al. Preoperative factors predict perioperative morbidity and mortality after pancreaticoduodenectomy. Ann Surg Oncol. 2011;18:2126–35. [DOI] [PubMed] [Google Scholar]
- 78. Sahakyan MA, Røsok BI, Kazaryan AM, et al. Impact of obesity on surgical outcomes of laparoscopic distal pancreatectomy: a Norwegian single‐center study. Surgery. 2016;160:1271–8. [DOI] [PubMed] [Google Scholar]
- 79. Dumitrascu T, Barbu ST, Purnichescu‐Purtan R, Ionescu M, Popescu I. Risk factors for surgical complications after central pancreatectomy. Hepatogastroenterology. 2012;59:592–8. [DOI] [PubMed] [Google Scholar]