Impact of High Body Mass Index on Outcomes of Laparoscopic Hysterectomy

Abstract

Objective:

The objective of this study was to investigate the association between obesity and intra/post–operative complications of total laparoscopic hysterectomy (TLH).

Materials and Methods:

This retrospective cohort study included 21,356 patients who underwent TLH and who were included in the National Surgical Quality Improvement Program database in 2016. Body mass index (BMI) was stratified according to the World Health Organization classifications (normal: 18.5–24.9 kg/m²; overweight: 25.0–29.9 kg/m²; obese I: 30–34.9 kg/m²; obese II: 35–39.9 kg/m²; obese III: ≥40 kg/m²). The primary outcome was the presence of intra/post–operative complications. Unadjusted and adjusted binary logistic regression was used to calculate odds ratios (ORs) and the corresponding 95% confidence intervals (CIs).

Results:

There was a statistically significant decrease in odds of complications in Obese I compared with normal weight (OR: 0.8; 95% CI 0.7–0.9). The subpopulations with increased odds of complications included postmenopausal patients (OR: 1.3; 95% CI 1.1–1.4); black patients (OR: 1.4; 95% CI 1.2–1.6); or patients with chronic hypertension (OR: 1.3; 95% CI 1.2–1.5), chronic obstructive pulmonary disease (OR: 1.9; 95% CI 1.3–2.8), disseminated cancer (OR: 2.8; 95% CI 1.8–4.2), and/or bleeding disorders (OR: 4.2; 95% CI 3.0–5.9).

Conclusions:

While obesity is a risk factor for developing comorbidities and increased surgical morbidity, it appears that a moderately high BMI may be protective in recovery. These findings support the “obesity paradox,” suggesting a counterintuitive benefit of adipose tissue when undergoing physiologic stress.

Introduction

Hysterectomy is one of the most common gynecologic surgical procedures in the United States, performed vaginally, abdominally, laparoscopically, or with robot-assisted laparoscopy. According to the recommendations of the American College of Obstetricians and Gynecologists, vaginal hysterectomy (VH) is the preferred approach to treat leiomyomas, abnormal uterine bleeding, pelvic organ prolapse, pelvic infection, or malignant disease.^1,2 Laparoscopic hysterectomy (LH) is commonly performed when VH is not feasible due to large uterus size, limited vaginal access, or other clinical factors determined by the physician.

Obesity, defined as a body mass index (BMI) of 30 kg/m² and above, is a major public health problem in the United States. The relationships between high BMI and increased risk of diabetes, coronary artery disease, hypertension, and hyperlipidemia have been well-characterized.³ In addition, high BMI has been linked to high surgical morbidity.⁴ However, the current scientific literature examining the effects of obesity on complications of hysterectomy is scant. Moreover, the current evidence has caused researchers to reach inconsistent conclusions.^5,6 For example, 1 of the largest studies including 55,409 patients who underwent hysterectomy for benign indications found that obesity was associated with longer operative times for abdominal, laparoscopic, and vaginal approaches.⁵ In contrast, a later study with 20,353 patients who underwent hysterectomy for benign indications demonstrated that the risks associated with high BMI largely depended on the route of surgery.⁶ Understanding the effects of obesity on outcomes of hysterectomy can help improve surgical management, postoperative care, and patient education.

The aim of this study was to investigate the association between obesity and intra/post–operative complications of total LH (TLH).

Materials and Methods

Study design

This was a retrospective cohort study, using secondary data from the American College of Surgeons National Surgical Quality Improvement Program (ACS NSQIP) 2016 database. Data provided from ACS NSQIP was obtained from medical records reviewed for patient demographics, presence of chronic conditions, and intra/post–operative complications.

Study population

This study reviewed data from a total of 21,843 patients, ages 18–89, who were admitted to a hospital to undergo a hysterectomy procedure (Current Procedural Terminology codes 58571 and 58573) in the year 2016. Patients with missing BMI data (n = 96) or patients with BMI <18.5 kg/m² (n = 391) were excluded from this study. The final sample included 21,356 patients.

Study variables

The main outcome variable, intra/post–operative complications, was created by combining data from several nominal variables. The intra/post–operative complications variable was defined, in combination, as return to the operating room, hospital readmission, length of stay for more than 2 days, transfusion (units), wound disruption, wound infection, postoperative Clostridium difficile colitis, sepsis, septic shock, urinary-tract infection, pneumonia, acute renal failure, stroke, pulmonary embolism, myocardial infarction, cardiac arrest requiring cardiopulmonary resuscitation, unplanned intubation, and/or death within 30 days.

The independent variable, BMI, was calculated by dividing body weight in lbs by height in inches (in) squared and multiplying by a conversion factor of 703. BMI was then categorized according to the established World Health Organization (WHO) criteria into normal weight (BMI: 18.5–24.9), overweight (BMI: 25.0–29.9), obese I (BMI: 30.0–34.9), obese II (BMI: 35–39.9), and obese III (BMI: ≥40.0).

Data for covariates were retrieved from clinical records. Age was measured in years and divided into three age categories as follows: (1) 18–39 (premenopausal); (2) 40–60 (perimenopausal); and (3) 61–89 (postmenopausal). Race was categorized into white, black, and other. Other included Asian, Native American, Alaska native, native Hawaiian, and Pacific Islander. Ethnicity was categorized as Hispanic versus non-Hispanic. Smoking status was determined by patients answering “Yes” or “No” to the question regarding whether they currently smoked within the past year. Presence of hypertension, diabetes mellitus (DM), chronic obstructive pulmonary disease (COPD), disseminated cancer, and bleeding disorder were also obtained from patients' clinical records.

Statistical analyses

Statistical analysis was performed using Stata software, release 14 Stata Corp, College Station, TX). Univariate analysis was performed for each variable to assess its distribution and proportion of missing data. Bivariate analysis, via a χ² test, was used to assess if the potential confounders were equally distributed according to the main exposure and outcome variables. Collinearity was assessed between all independent variables. Unadjusted and adjusted binary logistic regression models provided odds ratios (ORs) and 95% confidence intervals (CIs). A p-value <0.05 was considered to be statistically significant, and all statistical tests were 2-tailed.

Ethical considerations

The data sets used did not contain sensitive patient identifiers, and analysis of the data did not contain any sensitive information. Thus, this study was classified as non–human subject research and institutional review board approval was waived by the internal review board of the Florida International University Herbert Wertheim College of Medicine, in Miami, FL.

Results

A total of 21,356 patients were included in the final analysis, of which 21% (n = 4459) of patients had normal weight, 26.6% (n = 5687) of patients were overweight, 21.4% (n = 4577) of patients were obese I, 14.8% (n = 3157) of patients were obese II, and 16.3% (n = 3476) of patients were obese III. The average age of the sample size was 49. In patients undergoing TLH, 7% (n = 1705) of patients had complications and 92% (n = 19651) of patients did not have complications.

Table 1 shows the characteristics of the study participants undergoing TLH according to BMI categories. There was an increased percentage of postmenopausal women in the obese I, obese II, and obese III categories, compared with the normal and overweight categories. The percentage of black patients was highest among the obese I, obese II, and obese III categories, compared to white and other races (p-value <0.001). The percentages of patients with hypertension, DM, and bleeding disorders were statistically significantly higher in the obese I, obese II, and obese III categories (p-values <0.05).

Table 1.

Characteristics of Study Participants Undergoing TLH According to BMI Measured by kg/m² in Hospitals Participating in the ACS NSQIP in 2016

	BMI^a
	Normal weight	Overweight	Obese I	Obese II	Obese III
	(n = 4459)	(n = 5687)	(n = 4577)	(n = 3157)	(n = 3476)
Characteristics	%	%	%	%	%	p-Value
Age (in years)
18–39	20.9	18.6	19.7	20.8	20.3
40–60	63.2	64.0	60.5	59.0	57.7
61–89	16.0	17.5	19.8	20.1	22.1
Race						< 0.001
White	85.2	82.1	80.6	79.9	81.4
Black	5.7	11.9	15.6	17.1	16.3
Other	9.1	6.0	3.8	3.0	2.3
Ethnicity						< 0.001
Hispanic	7.9	11.9	11.7	9.3	7.5
Non-Hispanic	92.2	88.1	88.3	90.7	92.5
Current smoker^b						0.001
Yes	16.9	16.4	15.6	15.5	13.7
No	83.1	83.6	84.4	84.5	86.3
Hypertension^c						< 0.001
Yes	13.4	23.5	33.5	39.7	50.9
No	86.6	76.5	66.5	60.3	49.1
DM^d						< 0.001
Yes	2.6	5.9	10.8	15.6	22.2
No	97.4	94.1	89.3	84.5	77.8
History of COPD						0.02
Yes	1.0	1.0	1.0	1.2	1.6
No	99.0	99.1	99.0	98.8	98.4
Disseminated cancer						0.017
Yes	1.2	0.8	0.7	0.6	0.8
No	98.8	99.2	99.3	99.4	99.2
Bleeding disorders						0.003
Yes	0.7	0.7	0.9	1.0	1.4
No	99.4	99.3	99.1	99.0	98.7

BMI categories defined as normal, 18.5–24.9 kg/m²; overweight, 25–29.9 kg/m²; obese, I 30–34.9 kg/m²; obese II, 35–39.9 kg/m²; and obese III ≥40.0 kg/m².

Current smoker within 1-year.

Hypertension requiring medication.

Insulin-dependent and non–insulin-dependent diabetes.

TLH, total laparoscopic hysterectomy; ACS NSQIP, American College of Surgeons National Surgical Quality Improvement Program; BMI, body mass index; DM, diabetes mellitus; COPD, chronic obstructive pulmonary disease.

Table 2 shows the distribution of complications in TLH by BMI categories. Complications contributing most to the total percentages were hospital readmission, length of stays >2 days, and urinary-tract infection.

Table 2.

Distribution of Complication Types in TLH by BMI categories

BMI ^a
	Normal weight	Overweight	Obese I	Obese II	Obese III
Complication	n (%)	n (%)	n (%)	n (%)	n (%)
Return to OR	69 (18.8)	63 (14.3)	35 (10.6)	37 (15.3)	46 (14.2)
Hospital readmission	129 (35.1)	141 (32)	104 (31.6)	54 (22.3)	94 (28.9)
Length of stay for more than 2 days	105 (28.5)	139 (31.5)	122 (37.2)	95 (39.3)	120 (37.0)
Intra/post–operative transfusion (units)	42 (11.4)	55 (12.5)	39 (11.9)	35 (14.5)	29 (8.9)
Wound disruption	10 (2.7)	12 (2.7)	5 (1.5)	4 (1.7)	6 (1.9)
Wound infection	4 (1.1)	3 (0.7)	5 (1.5)	2 (0.8)	10 (3.1)
Postoperative Clostridium difficile colitis	4 (1.1)	6 (1.4)	3 (0.9)	4 (1.7)	4 (1.2)
Sepsis	12 (3.3)	18 (4.1)	22 (6.7)	10 (4.1)	12 (3.7)
Septic shock	1 (0.3)	3 (0.7)	2 (0.6)	3 (1.2)	6 (1.9)
UTI	101 (27.5)	113 (25.6)	84 (25.5)	64 (26.5)	83 (25.5)
Pneumonia	6 (1.6)	11 (2.5)	6 (1.8)	3 (1.2)	10 (3.1)
Acute renal failure	0 (0)	1 (0.2)	2 (0.6)	1 (0.4)	1 (0.3)
Stroke	1 (0.3)	1 (0.2)	1 (0.3)	1 (0.4)	2 (0.6)
Pulmonary embolism	13 (3.5)	15 (3.4)	12 (3.7)	4 (1.7)	9 (2.8)
Intra/post–operative MI	1 (0.3)	5 (1.1)	3 (0.9)	0 (0)	0 (0)
Intra/post–operative cardiac arrest requiring CPR	0 (0)	0 (0)	1 (0.3)	1 (0.4)	0 (0)
Intra/post–operative unplanned intubation	3 (0.8)	4 (0.9)	8 (2.4)	6 (2.5)	5 (1.5)
Intra/post-operative death within 30 days	1 (0.3)	4 (0.9)	1 (0.3)	1 (0.4)	3 (0.9)

BMI categories defined as: normal, 18.5–24.9 kg/m²; overweight, 25–29.9 kg/m²; obese I, 30–34.9 kg/m²; obese II, 35–39.9 kg/m²; and obese III ≥40.0 kg/m².

BMI, body mass index; TLH, total laparoscopic hysterectomy; OR, operating room; UTI, urinary-tract infection; MI, myocardial infarction; CPR, cardiopulmonary resuscitation.

Table 3 shows the unadjusted and adjusted associations between BMI categories and intra/post–operative complications in TLH. In the unadjusted analysis, no statistically significant association was found between BMI categories and intra/post–operative complications. After adjustment for patient demographics (age, race) and clinical risk factors (tobacco use, hypertension, DM, COPD, disseminated cancer, and bleeding disorders), there was a statistically significant decrease in odds of complications in obese I patients, compared with normal-weight patients (OR: 0.8; 95% CI: 0.7–0.9). In addition, there was a statistically significant increase in odds of complications in black patients (OR: 1.4; 95% CI 1.2–1.6), compared with white patients. Similarly, there were higher odds of complications in patients with hypertension (OR: 1.3; 95% CI 1.2–1.5), COPD (OR: 1.9; 95% CI 1.3–2.8), disseminated cancer (OR: 2.8; 95% CI 1.8–4.2), and bleeding disorders (OR: 4.2; 95% CI 3.0–5.9).

Table 3.

Unadjusted & Adjusted Associations Between BMI Categories & Intra/Post–Operative Complications in TLH in Hospitals Participating in the ACS NSQIP in 2016

	Complications ^a
	unadjusted	Adjusted
Characteristics	OR (95% CI)	OR (95% CI)
BMI^b
Normal	Ref. ^c	Ref. ^c
Overweight	0.9 (0.8–1.1)	1 (0.8–1.1)
Obese I	0.9 (0.7–1.0)	0.8 (0.7–0.9)
Obese II	0.9 (0.8–1.1)	0.8 (0.7–1.0)
Obese III	1.1 (1–1.3)	1 (0.8–1.1)
Age (in years)
18–39	1.2 (1.0–1.3)	1.2 (1.1–1.4)
40–60	Ref. ^c	Ref. ^c
61–89	1.5 (1.3–1.7)	1.3 (1.1–1.4)
Race
White	Ref.^c	Ref.^c
Black	1.4 (1.2–1.6)	1.4 (1.2–1.6)
Other	1.3 (1.1–1.7)	1.3 (1.1–1.7)
Current smoker^d
No	Ref.^c	Ref.^c
Yes	1.2 (1.0–1.3)	1.2 (1.0–1.3)
Hypertension^e
No	Ref.^c	Ref.^c
Yes	1.5 (1.3–1.6)	1.3 (1.2–1.5)
DM^f
No	Ref.^c	Ref.^c
Yes	1.4 (1.2–1.6)	1.1 (1.0–1.4)
History of COPD
No	Ref.^c	Ref.^c
Yes	2.2 (1.5–3.1)	1.9 (1.3–2.8)
Disseminated cancer
No	Ref.^c	Ref.^c
Yes	4.1 (2.9–5.8)	2.8 (1.8–4.2)
Bleeding disorders
No	Ref.^c	Ref.^c
Yes	4.7 (3.4–6.4)	4.2 (3.0–5.9)

Complications was defined as return to the operating room, hospital readmission, length of stay for more than 2 days, transfusion (units), wound disruption, wound infection, postoperative Clostridium difficile colitis, sepsis, septic shock, urinary tract infection, pneumonia, acute renal failure, stroke, pulmonary embolism, myocardial infarction, cardiac arrest requiring cardiopulmonary resuscitation, unplanned intubation, death within 30 days.

BMI categories defined as normal, 18.5–24.9 kg/m²; overweight, 25–29.9 kg/m²; obese I, 30–34.9 kg/m², obese II, 35–39.9 kg/m²; obese III, ≥40 kg/m².

Reference category.

Current smoker within 1-year.

Hypertension requiring medication.

Insulin-dependent and non–insulin dependent DM.

BMI, body mass index; TLH, total laparoscopic hysterectomy; ACS NSQIP, American College of Surgeons National Surgical Quality Improvement Program; OR, odds ratio; CI, confidence interval; DM, diabetes mellitus; COPD, chronic obstructive pulmonary disease.

Discussion

This study found that there was a statistically significant decrease in odds of complications in obese I, compared with normal BMI. In addition, the percentage of complications was highest among patients in the obese III category. The prevalence of complications was higher in postmenopausal patients, and in patients with histories of tobacco use, hypertension, DM, COPD, disseminated cancer, and bleeding disorders. Finally, patients who identified themselves as white had fewer complications, compared with patients who identified as black or other races.

Obesity has been linked to multiple comorbid conditions that diminish the overall health status of a patient.^3,7 However, it seems that a higher BMI paradoxically aids a body undergoing physiologic stress, whether it be iatrogenic or secondary to disease. Several studies throughout the years have reported this “obesity paradox” in complications for patients undergoing various medical procedures^8,9 or surviving chronic medical conditions.^10,11 It seems this paradox holds true more consistently as the population being studied becomes older,⁹ which is mirrored in the results of this present study. The mathematical model proposed to explain this relationship between BMI and mortality rate forms a U-shaped curve that becomes more prominent with age, which suggests that, as patients get older, the protective effects of a higher BMI are greater but only to a certain extent.¹² There are several hypotheses that are offered as attempts to explain this paradox, ranging from better baseline nutritional status and functional classification¹³ to misguided use of BMI as an oversimplified measure of obesity.¹⁴ At present, there is no clear consensus on the mechanism of this protective effect.

The results also showed that the percentage of black patients was highest in obese I, obese II, and obese III categories, compared to white patients and patients of other races, which mimics the trend measured across a 30-year span by the Centers for Disease Control and Prevention (CDC). According to the 2016 CDC Health Trend Table, black or African-American populations have had consistently higher percentages of overweight and obese individuals, compared to their white, Asian, and Hispanic/Latinx counterparts.¹⁵ Furthermore, in the current study, whites had a lower percentage of complications, compared to black and other races. Members of racial minority groups have been shown to be disproportionately affected by chronic disease, compared to their white counterparts, as well as suffering with a greater burden of disease. For example, according to the most recent estimates by the CDC in 2017, the age-adjusted prevalence of DM in American adults was higher among Native Americans/Alaska natives (15.1%), non-Hispanic blacks (12.7%), Hispanics (12.1%), and Asians (8.0%) than among non-Hispanic whites (7.4%).¹⁶

The increased likelihood of complications in black patients, compared with white patients could be a reflection of social determinants of health, including lower socioeconomic status and education level. As well as, lack of accessibility to health care and nutritious food impeding minority groups from receiving adequate medical care and proper nutrition, thus leading to an increased incidence of obesity and increasing the risk of complications further following surgical procedures. This is in line with the results published in the CDC Health Disparities and Inequalities Report in 2013.¹⁷ Additionally, studies have shown an inverse relationship between socioeconomic status and surgical risks, although expansion on this topic lay outside the scope of this study.¹⁸

The highest percentage of overall complications was seen among patients in the obese III category. In addition, there was a higher percentage of patients who had hypertension and DM in the obese I, obese II, and obese III categories. The results of the current study yielded a higher percentage of complications in patients with hypertension, DM, COPD, tobacco use, disseminated cancer, and bleeding disorders. Obesity is a multifactorial disease that is a well-known risk factor for the development of hypertension and DM due to maladaptive lifestyles, endocrine imbalances, vascular injuries, glomerular hyperfiltrations, and inflammatory responses. Hypertension and DM can have a negative impact on surgical outcomes by causing an increased risk of microvascular injury and multiorgan damage. This finding supports existing literature further that supported a relationship between high BMI and surgical morbidity.⁴ For example, obese patients who have DM might have impaired wound healing due to excess subcutaneous fat tissue leading to low regional perfusion and oxygen tension, as well as elevated blood glucose levels leading to impaired growth-factor production, macrophage function, fibroblast migration, and remodeling by matrix metalloproteinases.^19,20

Furthermore, patients with histories of COPD have increased risk of pulmonary complications such as intra/post–operative unplanned intubation and pneumonia.¹⁹ Similarly, chronic tobacco exposure can lead to transient decreased tissue oxygenation and long-term damage by dampening the inflammatory healing response via reduced inflammatory-cell chemotactic responses, migratory function, and oxidative bactericidal mechanisms.²¹ Patients with cancer and bleeding disorders have an inherent increased risk for intra/post–operative complications that might have a summative affect with added risks in obese patients.

The results also revealed that there was a higher percentage of patients with bleeding disorders in the 3 obese categories. While the relationship between obesity and bleeding risk remains unknown, this could be due to the chronic inflammatory state of obesity—mediated by tumor necrosis factor–α and interleukin 6–and impaired wound healing.²²

The results of this study suggest that low estrogen levels could contribute to physiologic mechanisms that promote fat storage in postmenopausal women. There was an increased percentage of postmenopausal women in the obese I, obese II, and obese III categories, compared to the normal and overweight categories. This is likely due to the effects of estrogen on adipose tissue storage and fatty-acid oxidation. In a 2013 study conducted at the Mayo Clinic, Rochester, MN, comparing adipose tissue in pre- and postmenopausal women of similar ages, researchers found that decreased estrogen levels led to the upregulation of adipocyte acyl-CoA synthetase and diacylglycerol acyltransferase activity, which correlated positively with free fatty-acid storage rates.²³

Some of the strength and novelty of this study includes the stratification of the obese category beyond the 30 kg/m² categories. Previous studies have defined obese as a BMI >30 kg/m², which likely misrepresented the findings, because patients with a BMI of 30–34.9 kg/m², 35–39.9 kg/m², or ≥40kg/m² might have different health outcomes, compared with patients with a BMI close to 30 kg/m². Thus, defining obesity as >30 kg/m² without any further categorization might miss important information. This study also utilized a database with an expansive array of variables not limited to demographics and also included comorbidities. This enabled analysis of many different possible confounders.

Naturally, this study had some limitations. First, was the availability of data, which restricted the pool of information to data that had been collected at the times the patients had the hysterectomies. More information about the patients' annual incomes, health literacy, and geographic locations (such as zip codes), would also have been pertinent to this study, given that these factors they are indirect measures of the social determinants of health and could have an effect on both BMI and operative complications.

Second, the data did not include the variability of surgeon expertise among the participating hospitals, which could have contributed to the complication rates.

Third, future studies should categorize complications into intraoperative complications, medical complications, and surgical complications in order to compare complication types among BMI categories, in accordance with a 2013 Journal of the American Medical Association study exploring in-house complication rates for hysterectomy.²⁴ By exploring the origins and etiologies of complications, medical providers could be more able to take steps to address these complications. The risk factors are changing in the face of minimally invasive procedures and improving technology, and further study a is needed to reassess these changes. Specific to gynecologic procedures, there are only a few studies that have explored these changes.

Conclusions

This study demonstrated a decrease in odds of intra/post–operative complications for TLH in obese I patients, compared with normal-weight patients. These results contribute to the growing body of literature that builds on the understanding of obesity. As the trend of BMI among the American population continues to increase, it is essential for physicians and scientists to expand the present scope of knowledge to care for overweight and obese patients. Over the years, the controversy surrounding the “obesity paradox” has led to much debate in the medical community and among the general population. To simplify the ambiguity surrounding this concept, it appears that obesity is a risk factor for developing chronic diseases and fatal events; however, once those events have occurred, a higher BMI may be an alleviating factor in recovery. That said, further investigation is needed to explore future weight management of older patients, especially those with chronic conditions.

Footnotes

Acknowledgements

We would like to thank the ACS NSQIP 2016 for allowing us to utilize their database.

Author Disclosure Statement

No financial conflicts of interest exist.

References

Committee on Gynecologic Practice. Matteson

, Butts

. Committee Opinion No 701: Choosing the Route of Hysterectomy for Benign Disease. Obstet Gynecol, 2017; 129:155.

Aarts

, Nieboer

, Johnson

, Tavender

, Garry

, Moi

, Kluivers

. Surgical approach to hysterectomy for benign gynaecological disease. Cochrane Database Syst Rev, 2015; 8:CD003677.

O'Hanlan

, Lopez

, Dibble

, Garnier

, Huang

, Leuchtenberger

. Total laparoscopic hysterectomy: Body mass index and outcomes. Obstet Gynecol, 2003; 102:1384.

Choban

, Flancbaum

. The impact of obesity on surgical outcomes: A review. J Am Coll Surg, 1997; 185:593.

Shah

, Vitonis

, Missmer

. Association of body mass index and morbidity after abdominal, vaginal, and laparoscopic hysterectomy. Obstet Gynecol, 2015; 125:589.

Osler

, Daugbjerg

, Frederiksen

, Ottesen

. Body mass and risk of complications after hysterectomy on benign indications. Hum Reprod, 2011; 26:1512.

GBD 2015 Obesity Collaborators; Afshin

, Forouzanfar

, Reitsma

, et al. Health effects of overweight and obesity in 195 countries over 25 years. N Engl J Med, 2017; 377:13.

Shaparin

, Widyn

, Nair

, Kho

, Geller

, Delphin

. Does the obesity paradox apply to early postoperative complications after hip surgery? A retrospective chart review. J Clin Anesth, 2016; 32:84.

Tulinský

, Mitták

, Tomášková

, Ostruszka

, Penka

, Ihnát

. Obesity paradox in patients undergoing lung lobectomy—myth or reality?. BMC Surg, 2018; 18:61.

10.

Das

, Alexander

, Chen

, et al. Impact of body weight and extreme obesity on the presentation, treatment, and in-hospital outcomes of 50,149 patients with ST-Segment elevation myocardial infarction results from the NCDR (National Cardiovascular Data Registry). J Am Coll Cardiol, 2011; 58:2642.

11.

Horwich

, Fonarow

, Hamilton

, MacLellan

, Woo

, Tillisch

. The relationship between obesity and mortality in patients with heart failure. J Am Coll Cardiol, 2001; 38:789.

12.

Childers

, Allison

. The ‘obesity paradox’: A parsimonious explanation for relations among obesity, mortality rate, and aging?. Int J Obes (Lond), 2010; 34:1231.

13.

Goyal

, Nimmakayala

, Zonszein

. Is there a paradox in obesity?. Cardiol Rev, 2014; 22:163.

14.

Casas-Vara

, Santolaria

, Fernández-Bereciartúa

, González-Reimers

, Garcia-Ochoa

, Martinez-Riera

. The obesity paradox in elderly patients with heart failure: Analysis of nutritional status. Nutrition, 2012; 28:616.

15.

National Center for Health Statistics (US). Health, United States, 2016: With Chartbook on Long-Term Trends in Health. Hyattsville, MD: National Center for Health Statistics. 2017. Online document at: www.ncbi.nlm.nih.gov/books/NBK453378/ Accessed November 23, 2018.

16.

Centers for Disease Control and Prevention (CDC). National Diabetes Statistics Report | Data & Statistics | Diabetes | CDC. Online document at: www.cdc.gov/diabetes/data/statistics/statistics-report.html Published May 15, 2018. Accessed November 23, 2018.

17.

Centers for Disease Control and Prevention (CDC). Introduction: CDC Health Disparities and Inequalities Report—United States, 2013. Online document at: www.cdc.gov/mmwr/preview/mmwrhtml/su6203a2.htm Accessed November 23, 2018.

18.

Chong

, Imhoff

, Harken

. Socioeconomic status and the assessment of operative risk. Surgery, 2015; 157:605.

19.

Tjeertes

, Hoeks

, Beks

, Valentijn

, Hoofwijk

, Stolker

. Obesity—a risk factor for postoperative complications in general surgery?. BMC Anesthesiol, 2015; 15:112.

20.

Brem

, Tomic-Canic

. Cellular and molecular basis of wound healing in diabetes. J Clin Invest, 2007; 117:1219.

21.

Sørensen

. Wound healing and infection in surgery: The pathophysiological impact of smoking, smoking cessation, and nicotine replacement therapy. A systematic review. Ann Surg, 2012; 255:1069.

22.

Ellulu

, Patimah

, Khaza'ai

, Rahmat

, Abed

. Obesity and inflammation: The linking mechanism and the complications. Arch Med Sci, 2017; 13:851.

23.

Santosa

, Jensen

. Adipocyte fatty acid storage factors enhance subcutaneous fat storage in postmenopausal women. Diabetes, 2013; 62:775.

24.

Wright

, Ananth

, Lewin

, et al. Robotically assisted vs laparoscopic hysterectomy among women with benign gynecologic disease. JAMA, 2013; 309:689.