RECONSTRUCTIVE SURGERY
Predictive Value of Nutritional Markers for Wound Healing Complications in Bariatric Patients Undergoing Panniculectomy John Richard Barbour, MD,* Matthew L. Iorio, MD,* Christine Oh, MS,* Thomas H. Tung, MD,Þ and Patrick J. O’Neill, MDþ Background: Hypoproteinemia and nutritional deficiencies are common after bariatric surgery, and although massive weight loss (MWL) patients experience increased wound complication rates, the association has not been causatively determined. Objectives: This study investigated preoperative nutritional parameters and wound complications in MWL patients (postbariatric and diet-controlled) undergoing panniculectomy at 2 academic institutions. Methods: One hundred sixty-one consecutive patients undergoing elective panniculectomy after bariatric surgery or diet-controlled weight loss were identified. Patient demographics and nutritional indices (serum protein, albumin, and micronutrient levels) were analyzed. Complications including wound separation, infection, and operative debridements were compared. Post hoc comparisons tested for correlation between complications and nutritional markers. Results: Postbariatric patients lost an average of 151 lb and presented at an average of 32 months after gastric bypass. Diet-controlled weight loss patients lost an average of 124 lb. Despite MWL, albumin levels were higher in the bariatric group (3.8 vs 3.4 g/dL, P G 0.05). Conversely, bariatric patients experienced increased wound complications (27% vs 14%; P G 0.05). Factors which were found to correlate to increased risk of wound dehiscence and infection were elevated body mass index at time of panniculectomy and amount of tissue removed. Multivariate analysis did not show serum albumin or percent weight loss to independently predict complications. Conclusions: Bariatric patients presenting for elective operations are at risk for protein and micronutrient deficiency. Despite aggressive replacement and normalization of nutritional markers, bariatric patients experience increased wound complications when compared to nonbariatric patients and traditional measures of nutritional evaluation for surgery may be insufficient in bariatric patients. Key Words: obesity, bariatric surgery, wound healing, massive weight loss, dietetics (Ann Plast Surg 2015;75: 435Y438)
D
emographics from the Centers for Disease Control demonstrate that more than one third of US adults (35.7%) are obese. As this percentage continues to grow, a rise in bariatric surgery has been noted with a 6-fold increase in weight-loss surgeries.1,2 This has led to a rise in body contouring procedures after massive weight loss (MWL). Received June 17, 2013, and accepted for publication, after revision, February 3, 2014. From the *Department of Plastic Surgery, Georgetown University Hospital, Washington, DC; †Washington University School of Medicine, St Louis, MO; and ‡Medical University of South Carolina, Charleston, SC. Barbour JR, attending surgeon, study design, and data collection; Iorio ML, manuscript preparation and data collection; Oh C, manuscript preparation and data collection; Tung TH, attending surgeon; O’Neill PJ, attending surgeon and study design. Conflicts of interest and sources of funding: none declared. Reprints: John Richard Barbour, MD, Department of Plastic Surgery, Georgetown University Hospital, 3800 Reservoir Rd, NW, PHC, 1st Floor Washington, DC 20007. E-mail: [email protected]. Copyright * 2014 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0148-7043/15/7504-0435 DOI: 10.1097/SAP.0000000000000188
Annals of Plastic Surgery
& Volume 75, Number 4, October 2015
According to the American Society of Plastic Surgeons, approximately 45,000 body contouring procedures after MWL were performed in 2012.3 However, body contouring procedures after MWL are noted to have an increased rate of wound healing complications as compared to nonbariatric patients, with complication rates of 41% and 22%, respectively.4,5 Hypoproteinemia and nutritional deficiencies are common after bariatric surgery, and although MWL patients experience high wound complication rates, the association has not been causatively determined.6 Factors that impact wound healing include malnutrition (decreased protein stores and micronutrients, increased general malabsorption), skin dysfunction (decreased elasticity and impaired microcirculation) and inf lammation (increased matrix metalloproteinases and interleukins). Progressive and persistent protein deficiency after bariatric surgery may contribute to poor healing secondary to reduced collagen formation and diminished wound strength.7 Specifically, correlations between postbariatric surgery and body contouring complications are based on the presumptive low-protein reserve due to malabsorption, and the manifestation through wound healing complications.8 However, these reports are largely associative, and emerging data indicate that current albumin and prealbumin guidelines are inadequate for predicting wound-based complications after body contouring. This study evaluated the efficacy of structured postbariatric nutritional supplementation programs in normalizing nutritional markers and investigated the relationship between preoperative nutritional parameters and wound complications in MWL patients in both postbariatric and diet-controlled weight loss patients undergoing panniculectomy at multiple academic institutions.
METHODS After institutional review board approval, a retrospective review was performed on all consecutive patients from January 2005 to December 2010 who presented for panniculectomy after either bariatric surgery or diet-controlled weight loss. One hundred sixty-one consecutive patients were identified. Patient demographics including medical comorbidities, etiology of weight loss, total and percentage weight loss, and nutritional indices (serum protein, albumin, and micronutrient levels) were recorded. All complications were recorded. Complications that included any wound separation, infection, and/or operative debridements were grouped, and a subgroup comparison was performed between the 2 cohorts. Post hoc comparisons tested for correlation between complications and nutritional markers. Patients were excluded if preoperative serum nutritional measurements could not be obtained, or if clinical follow-up was less than 6 months after panniculectomy. Similarly, patients who presented for panniculectomy without a recent or sustained weight loss through diet/ exercise or gastric bypass were excluded. Statistical analyses were performed using STATA 12 (STATACorp, College Station, Tex). Means and standard deviations are used to report continuous data. Complications and other patient characteristics are reported as frequencies and rates. Multivariate analysis was performed using analysis of variance. Statistical significance for all tests was established at 0.05, using 2-tailed tests. www.annalsplasticsurgery.com
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RESULTS Between January 2005 and December 2009, a total of 161 patients presented for infraumbilical panniculectomy after MWL at 2 major teaching hospitals. Of these, 124 (77%) patients had undergone gastric bypass before panniculectomy, and 37 (23%) patients had used diet/exercise for weight loss. Of those undergoing gastric bypass, 110 (89%) patients had undergone laparoscopic procedures compared to 14 (11%) patients who had an open vertical midline approach. No patients underwent true umbilical transposition, but 31 (25%) patients from the gastric bypass group and 14 (38%) of the diet/exercise group underwent a vertical Fleur-de-lisYtype component for adequate skin resection, and this required resetting of the umbilicus within the vertical incision. The 2 groups were equal in composition of sex (83% and 85% female, respectively) and age (42.6 and 40.5 years, respectively). Associated comorbidities of hypertension, active tobacco use, or diabetes mellitus also did not differ between the 2 groups (Table 1). Postbariatric patients lost an average of 151 lb and presented at an average of 32 months after gastric bypass. Diet-controlled weight loss patients lost an average of 124 lb before presentation. Despite MWL, albumin levels were higher in the gastric-bypass group (3.8 vs 3.4 g/dL, P G 0.05). Conversely, gastric-bypass patients experienced a significantly increased rate of wound complications (27% vs 14%, P G 0.05). Factors that were found to correlate with the increased risk of wound dehiscence and infection were elevated body mass index (BMI) at time of panniculectomy and volume of tissue removed. Ventral hernia was encountered and repaired in 15 (9%) patients, and was most commonly the result of a previous lower transverse incision. These hernias did not show a statistical relation to wound healing problems and there was no reported incidence of known recurrence in these 15 patients. Although more patients from the diet/exercise group did have a vertical component to the skin resection (38% vs 25%), this did not show an increased risk of wound healing despite the longer incision and wound closure. Multivariate analysis did not show serum albumin or percent weight loss to independently predict complications (Table 2).
DISCUSSION Despite the frequent improvement of medical comorbidities after MWL, previously obese patients are left with the stigmata of redundant skin. It is not surprising that the popularity of body contouring surgery has mirrored the rising trend of bariatric surgeries.3 Nearly, three quarters (74%) of postbariatric patients desire body-contouring surgery and abdominal contouring procedures including both panniculectomy and formal abdominoplasty are the most popular (59%).9 Unfortunately, body-contouring procedures are often associated with wound healing complications such as infection (16%Y48%), skin necrosis (6%Y10%), and wound dehiscence (13%Y33%).5 Although the number of patients presenting for body contouring after MWL continues to rise, there are no definitive guidelines on how to improve postsurgical outcomes. This
& Volume 75, Number 4, October 2015
TABLE 2. Preoperative Nutritional Comparison Between the Gastric Bypass and Nongastric Bypass Study Groups
Serum albumin, g/dL Serum prealbumin, mg/dL Hemoglobin level, mg/dL Serum iron, Hg/dL Serum calcium, mg/dL Serum glucose, mg/dL
Gastric Bypass (n = 124)
Nongastric Bypass (n = 37)
3.6 20.1 36.0 74 8.2 121
3.1* 14.7* 38.2 52 7.1 118
*Statistically significant difference at a P G 0.05.
study focused on the preoperative nutritional parameters and postsurgical complications of patients who underwent panniculectomy after MWL through either bariatric surgery or diet-controlled weight loss. It is worth noting that this is a retrospective analysis of 3 surgeon’s practices, with minor variances in patient selection and surgical techniques; however, multiple findings were consistent across each patient cohort. Despite increased serum protein markers, aggressive supplemental replacement and normalization of nutritional markers, the postbariatric group experienced increased rates of wound complications when compared to nonbariatric patients undergoing similar procedures (Figs. 1 and 2). A subgroup analysis of postbariatric patients did not show low albumin levels to be an accurate predictor of complications or reoperation. Two factors that were found to correlate with the increased risk of wound dehiscence and infection were elevated BMI at the time of panniculectomy and the amount of tissue removed. Multivariate analysis did not show serum albumin or percent weight loss to independently predict complications. Postbariatric patients frequently develop malnutrition given that the most common procedure, Roux-en-Y gastric bypass, combines both restrictive and malabsorptive aspects of bariatric surgery. Nutritional deficiency after bariatric surgery can be categorized into 3 types as follows: (1) vitamin/mineral deficiencies, (2) dehydration, and (3) protein-energy malnutrition.10 Among the vitamin and mineral deficiencies, iron deficiency after Roux-en-Y gastric bypass is especially common, as the usual sites of iron absorption, the duodenum and proximal jejunum, are no longer involved in the absorptive phase. Most germain to wound healing complications, though, is protein intolerance.
TABLE 1. Patient Demographics and Comparison of Associated Comorbidities
BMI, kg/m2 Age, y Time from surgery, mo Total weight loss, lb Weight of pannus removed, lb Active tobacco use, % Active diabetes, % Active hypertension, %
436
Gastric Bypass (n = 124)
Nongastric Bypass (n = 37)
33.8 42.6 32.1 142.1 24.1 8 37 10
36.4 40.5 V 124.2 19.7 10 44 9
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FIGURE 1. A 55-year-old woman underwent a 4650-g abdominal panniculectomy after diet-controlled weight loss. The superior vertical component was left open and negative pressure wound therapy was applied to decrease seroma formation. * 2014 Wolters Kluwer Health, Inc. All rights reserved.
Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Annals of Plastic Surgery
& Volume 75, Number 4, October 2015
FIGURE 2. The same patient 9 days after abdominal panniculectomy, with complete dehiscence of her wound due to skin and fat necrosis. Of note, her albumin level was 3.3 g/dL before the initial operation.
In the absence of supplementation, protein malnutrition can develop.8 With rapid weight loss, the amino acid pool is diverted to gluconeogenesis, which, in combination with malabsorption and intolerance to high-protein foods, can lead to protein depletion.11 Protein deficiency inhibits maximal wound healing by impairing DNA production, neovascularization, fibroblast proliferation, collagen synthesis, and wound remodeling. Hypoproteinemia can also lead to decreased oxygenation and nutrient transport to the wound secondary to edema formation.12 Protein deficiency is traditionally recognized by low serum albumin, which indicates the depletion of total body proteins.13 Serum albumin concentrations of 3.5 g/dL or greater are considered normal; the values for mild, moderate, and severe depletion are 3.5Y2.8, 2.7Y2.1, and less than 2.1 g/dL, respectively.14 A plethora of published literature exists showing low serum albumin levels as a strong predictor for adverse surgical outcomes. A decrease in serum albumin from 4.6 to less than 2.1 g/dL is associated with an increase in postoperative sepsis and major infections.15 There are many studies that have stressed the importance of optimal nutrition before reconstructive surgery8,16Y18 and the utility of serum albumin levels, but our results indicate that there may not be a causative link between albumin levels and perioperative complications in MWL patients. Despite higher average albumin levels before surgery (3.8 vs 3.4 g/dL) and lower percent of albumin less than 3.5 g/dL (26% vs 50%), our bariatric patients had increased rates of wound complications after panniculectomy when compared to diet-controlled patients with lower albumin levels (WS, 27% vs 14%; WI, 26% vs 16%; P G 0.05). These findings correlate with those of Larson et al,19 who performed a 5-year retrospective chart review of 101 patients with 179 pressure ulcers, and unlinked patients’ preoperative nutritional status and investigated the rates of recurrence and complications. Neither admission prealbumin nor albumin levels were associated with 2-year recurrence or complications of pressure ulcers. Serum albumin and prealbumin levels were found to have significantly increased upon discharge and wound closure, indicating that large open wounds result in significant protein loss secondary to a chronic inf lammatory state. Due to the impracticality of admitting patients solely for nutritional supplementation and monitoring, they established a protocol with lower recurrence and complication rates of 16.8% and 17% compared to published rates of 12% to 82% and 16% to 46%.19 Specific factors which were found to correlate to increased risk of wound dehiscence and infection were elevated BMI at time of panniculectomy and volume of tissue removed. Previous associations between BMI, amount of tissue removed, and adverse outcomes are * 2014 Wolters Kluwer Health, Inc. All rights reserved.
Nutritional Markers in Wound Healing Complications
well documented.20Y22 A retrospective analysis by Vastine et al23 demonstrated an 80% complication rate for obese patients after abdominoplasty compared to the 33% and 32.5% for borderline obese and nonobese cohorts, respectively. Coon et al21 demonstrated in a prospective study of 449 bariatric patients undergoing body contouring that elevated BMI at the time of surgery was a predictor of complications. A retrospective study by Neaman and Hansen20 found a positive correlation between greater volumes of tissue removed and increased wound infections and dehiscence. With successful weight loss, a patient with a higher initial BMI who loses more weight is expected to have greater deformities requiring more extensive operations, which is ref lected in our study. Efforts to curtail complications and improve outcomes include perioperative attention to the medical comorbidities of the obese and MWL groups. Heart disease, hypertension, dyslipidemia, diabetes, obstructive sleep apnea, gastroesophageal reflux disease, and osteoarthritis are common comorbid conditions,24 generating increased postoperative complications of wound infections,25 pulmonary complications,26 thromboembolic events27 and increased mortality.28 The risk of surgical complications for associated morbidities seems to decrease as the patient’s BMI normalizes. Current best-practice recommendations include the delay of body-contouring surgery until the postbariatric or MWL patient has been weight stable for a period of 2 months, often corresponding to 12 to 18 months after gastric bypass.24 The best candidates for extensive body contouring have a BMI in the range of 25 to 30 kg/m2. This allows the patient to reach metabolic and nutritional homeostasis and better aesthetic outcomes upon reaching a stable weight.24 In our analysis, postbariatric patients presented at an average of 32 months after gastric bypass with a BMI of 33.8 kg/m2 and nongastric bypass patients with a higher BMI of 36.4 kg/m2. Both groups reached a stable maintenance weight before panniculectomy, yet the postbariatric group still had a greater rate of complications, even with a lower preoperative BMI. MWL patients do have significant nutritional deficiencies, and infraumbilical panniculectomy is known to have higher perioperative complication rates than other elective surgeries. We support that supplementation should be of benefit given evidence of the importance of protein in the wound healing process, but patients who are weightstable may still have tenuous protein and energy intake. Major elective surgery such as panniculectomy and abdominal contouring requires an increased energy and protein consumption of approximately 25%.29 Protein malnutrition in the bariatric population is difficult to diagnose and although the medical community has traditionally used serum albumin levels to reflect protein deficiency, current recommendations that have extrapolated a link between albumin levels and perioperative complications may be misleading.
CONCLUSIONS Despite being reported in the literature, associations between serum albumin and postoperative wound healing complications may not demonstrate a direct causative relationship. Variables that have increased predictive value for postoperative complications include an elevated BMI at time of surgery, as well as tissue resection volumes above 10 kg. Nutritional optimization should remain a cornerstone of appropriate perioperative management, however, patients with increased BMI or planned tissue resection volumes should be expectantly managed for postoperative wound healing complications. These data may provide increased evidence for staged resections with decreased wound tension or tissue trauma at the time of skin resection procedures. Accordingly, there is a need for further studies looking at other associated nutritional measures. In this way, patient outcomes can be optimized while minimizing avoidable surgical complications. REFERENCES 1. Trus TL, Pope GD, Finlayson SR. National trends in utilization and outcomes of bariatric surgery. Surg Endosc. 2005;19:616Y620.
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2. Ogden CCM, Kit BK, Flegal K. Centers for Disease Control and Prevention. Prevalence of Obesity in the United States, 2009-2010. 2009-2010. Accessed Accessed May 15, 2013. 3. Surgeons ASoP. Procedural Statistics, 2012. Available at: http://www.plasticsurgery.org/ Documents/news-resources/statistics/2012-Plastic-Surgery-Statistics/body-contouringafter-massive-weight-loss.pdf. Accessed May 15, 2013. 4. Greco JA 3rd, Castaldo ET, Nanney LB, et al. The effect of weight loss surgery and body mass index on wound complications after abdominal contouring operations. Ann Plast Surg. 2008;61:235Y242. 5. Acarturk TO, Wachtman G, Heil B, et al. Panniculectomy as an adjuvant to bariatric surgery. Ann Plast Surg. 2004;53:360Y366; discussion 367. 6. Naghshineh N, O’Brien Coon D, McTigue K, et al. Nutritional assessment of bariatric surgery patients presenting for plastic surgery: a prospective analysis. Plast Reconstr Surg. 2010;126:602Y610. 7. Russell L. The importance of patients’ nutritional status in wound healing. Br J Nurs. 2001;10(suppl 6):S42, S44YS49. 8. Agha-Mohammadi S, Hurwitz DJ. Enhanced recovery after body-contouring surgery: reducing surgical complication rates by optimizing nutrition. Aesthetic Plast Surg. 2010;34:617Y625. 9. Kitzinger HB, Abayev S, Pittermann A, et al. The prevalence of body contouring surgery after gastric bypass surgery. Obes Surg. 2012;22:8Y12. 10. Kaafarani HM, Shikora SA. Nutritional support of the obese and critically ill obese patient. Surg Clin North Am. 2011;91:837Y855, viii-ix. 11. Moize V, Geliebter A, Gluck ME, et al. Obese patients have inadequate protein intake related to protein intolerance up to 1 year following Roux-en-Y gastric bypass. Obes Surg. 2003;13:23Y28. 12. Hess CT. Monitoring laboratory values: protein and albumin. Adv Skin Wound Care. 2009;22:48. 13. Sebastian JL. Bariatric surgery and work-up of the massive weight loss patient. Clin Plast Surg. 2008;35:11Y26. 14. Grant JP, Custer PB, Thurlow J. Current techniques of nutritional assessment. Surg Clin North Am. 1981;61:437Y463. 15. Gibbs J, Cull W, Henderson W, et al. Preoperative serum albumin level as a predictor of operative mortality and morbidity: results from the National VA Surgical Risk Study. Arch Surg. 1999;134:36Y42.
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16. Araco A, Gravante G, Araco F, et al. Body contouring after weight loss: the plastic-bariatric surgery symbiosis. Aesthetic Plast Surg. 2006;30:374Y376. 17. Shermak MA, Chang D, Magnuson TH, et al. An outcomes analysis of patients undergoing body contouring surgery after massive weight loss. Plast Reconstr Surg. 2006;118:1026Y1031. 18. Ruberg RL. Role of nutrition in wound healing. Surg Clin North Am. 1984; 64:705Y714. 19. Larson DL, Hudak KA, Waring WP, et al. Protocol management of late-stage pressure ulcers: a 5-year retrospective study of 101 consecutive patients with 179 ulcers. Plast Reconstr Surg. 2012;129:897Y904. 20. Neaman KC, Hansen JE. Analysis of complications from abdominoplasty: a review of 206 cases at a university hospital. Ann Plast Surg. 2007;58:292Y298. 21. Coon D, Gusenoff JA, Kannan N, et al. Body mass and surgical complications in the postbariatric reconstructive patient: analysis of 511 cases. Ann Surg. 2009;249:397Y401. 22. Arthurs ZM, Cuadrado D, Sohn V, et al. Post-bariatric panniculectomy: prepanniculectomy body mass index impacts the complication profile. Am J Surg. 2007;193:567Y570; discussion 570. 23. Vastine VL, Morgan RF, Williams GS, et al. Wound complications of abdominoplasty in obese patients. Ann Plast Surg. 1999;42:34Y39. 24. Rubin JP, Toy J. Discussion. Prospective assessment of nutrition and exercise parameters before body contouring surgery: optimizing attainability in the massive weight loss population. Plast Reconstr Surg. 2010;125:1248Y1249. 25. Thomas EJ, Goldman L, Mangione CM, et al. Body mass index as a correlate of postoperative complications and resource utilization. Am J Med. 1997;102: 277Y283. 26. Gould AB Jr. Effect of obesity on respiratory complications following general anesthesia. Anesth Analg. 1962;41:448Y452. 27. Colwell CW Jr, Collis DK, Paulson R, et al. Comparison of enoxaparin and warfarin for the prevention of venous thromboembolic disease after total hip arthroplasty. Evaluation during hospitalization and three months after discharge. J Bone Joint Surg Am. 1999;81:932Y940. 28. Prem KA, Mensheha N, McKelvey JL. Operative treatment of adenocarcinoma of the endometrium in obese women. Am J Obstet Gynecol. 1965;92:16Y22. 29. Van Way CW 3rd. Nutritional support in the injured patient. Surg Clin North Am. 1991;71:537Y548.
* 2014 Wolters Kluwer Health, Inc. All rights reserved.
Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Predictive Value of Nutritional Markers for Wound Healing Complications in Bariatric Patients Undergoing Panniculectomy John Richard Barbour, MD,* Matthew L. Iorio, MD,* Christine Oh, MS,* Thomas H. Tung, MD,Þ and Patrick J. O’Neill, MDþ Background: Hypoproteinemia and nutritional deficiencies are common after bariatric surgery, and although massive weight loss (MWL) patients experience increased wound complication rates, the association has not been causatively determined. Objectives: This study investigated preoperative nutritional parameters and wound complications in MWL patients (postbariatric and diet-controlled) undergoing panniculectomy at 2 academic institutions. Methods: One hundred sixty-one consecutive patients undergoing elective panniculectomy after bariatric surgery or diet-controlled weight loss were identified. Patient demographics and nutritional indices (serum protein, albumin, and micronutrient levels) were analyzed. Complications including wound separation, infection, and operative debridements were compared. Post hoc comparisons tested for correlation between complications and nutritional markers. Results: Postbariatric patients lost an average of 151 lb and presented at an average of 32 months after gastric bypass. Diet-controlled weight loss patients lost an average of 124 lb. Despite MWL, albumin levels were higher in the bariatric group (3.8 vs 3.4 g/dL, P G 0.05). Conversely, bariatric patients experienced increased wound complications (27% vs 14%; P G 0.05). Factors which were found to correlate to increased risk of wound dehiscence and infection were elevated body mass index at time of panniculectomy and amount of tissue removed. Multivariate analysis did not show serum albumin or percent weight loss to independently predict complications. Conclusions: Bariatric patients presenting for elective operations are at risk for protein and micronutrient deficiency. Despite aggressive replacement and normalization of nutritional markers, bariatric patients experience increased wound complications when compared to nonbariatric patients and traditional measures of nutritional evaluation for surgery may be insufficient in bariatric patients. Key Words: obesity, bariatric surgery, wound healing, massive weight loss, dietetics (Ann Plast Surg 2015;75: 435Y438)
D
emographics from the Centers for Disease Control demonstrate that more than one third of US adults (35.7%) are obese. As this percentage continues to grow, a rise in bariatric surgery has been noted with a 6-fold increase in weight-loss surgeries.1,2 This has led to a rise in body contouring procedures after massive weight loss (MWL). Received June 17, 2013, and accepted for publication, after revision, February 3, 2014. From the *Department of Plastic Surgery, Georgetown University Hospital, Washington, DC; †Washington University School of Medicine, St Louis, MO; and ‡Medical University of South Carolina, Charleston, SC. Barbour JR, attending surgeon, study design, and data collection; Iorio ML, manuscript preparation and data collection; Oh C, manuscript preparation and data collection; Tung TH, attending surgeon; O’Neill PJ, attending surgeon and study design. Conflicts of interest and sources of funding: none declared. Reprints: John Richard Barbour, MD, Department of Plastic Surgery, Georgetown University Hospital, 3800 Reservoir Rd, NW, PHC, 1st Floor Washington, DC 20007. E-mail: [email protected]. Copyright * 2014 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0148-7043/15/7504-0435 DOI: 10.1097/SAP.0000000000000188
Annals of Plastic Surgery
& Volume 75, Number 4, October 2015
According to the American Society of Plastic Surgeons, approximately 45,000 body contouring procedures after MWL were performed in 2012.3 However, body contouring procedures after MWL are noted to have an increased rate of wound healing complications as compared to nonbariatric patients, with complication rates of 41% and 22%, respectively.4,5 Hypoproteinemia and nutritional deficiencies are common after bariatric surgery, and although MWL patients experience high wound complication rates, the association has not been causatively determined.6 Factors that impact wound healing include malnutrition (decreased protein stores and micronutrients, increased general malabsorption), skin dysfunction (decreased elasticity and impaired microcirculation) and inf lammation (increased matrix metalloproteinases and interleukins). Progressive and persistent protein deficiency after bariatric surgery may contribute to poor healing secondary to reduced collagen formation and diminished wound strength.7 Specifically, correlations between postbariatric surgery and body contouring complications are based on the presumptive low-protein reserve due to malabsorption, and the manifestation through wound healing complications.8 However, these reports are largely associative, and emerging data indicate that current albumin and prealbumin guidelines are inadequate for predicting wound-based complications after body contouring. This study evaluated the efficacy of structured postbariatric nutritional supplementation programs in normalizing nutritional markers and investigated the relationship between preoperative nutritional parameters and wound complications in MWL patients in both postbariatric and diet-controlled weight loss patients undergoing panniculectomy at multiple academic institutions.
METHODS After institutional review board approval, a retrospective review was performed on all consecutive patients from January 2005 to December 2010 who presented for panniculectomy after either bariatric surgery or diet-controlled weight loss. One hundred sixty-one consecutive patients were identified. Patient demographics including medical comorbidities, etiology of weight loss, total and percentage weight loss, and nutritional indices (serum protein, albumin, and micronutrient levels) were recorded. All complications were recorded. Complications that included any wound separation, infection, and/or operative debridements were grouped, and a subgroup comparison was performed between the 2 cohorts. Post hoc comparisons tested for correlation between complications and nutritional markers. Patients were excluded if preoperative serum nutritional measurements could not be obtained, or if clinical follow-up was less than 6 months after panniculectomy. Similarly, patients who presented for panniculectomy without a recent or sustained weight loss through diet/ exercise or gastric bypass were excluded. Statistical analyses were performed using STATA 12 (STATACorp, College Station, Tex). Means and standard deviations are used to report continuous data. Complications and other patient characteristics are reported as frequencies and rates. Multivariate analysis was performed using analysis of variance. Statistical significance for all tests was established at 0.05, using 2-tailed tests. www.annalsplasticsurgery.com
Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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RESULTS Between January 2005 and December 2009, a total of 161 patients presented for infraumbilical panniculectomy after MWL at 2 major teaching hospitals. Of these, 124 (77%) patients had undergone gastric bypass before panniculectomy, and 37 (23%) patients had used diet/exercise for weight loss. Of those undergoing gastric bypass, 110 (89%) patients had undergone laparoscopic procedures compared to 14 (11%) patients who had an open vertical midline approach. No patients underwent true umbilical transposition, but 31 (25%) patients from the gastric bypass group and 14 (38%) of the diet/exercise group underwent a vertical Fleur-de-lisYtype component for adequate skin resection, and this required resetting of the umbilicus within the vertical incision. The 2 groups were equal in composition of sex (83% and 85% female, respectively) and age (42.6 and 40.5 years, respectively). Associated comorbidities of hypertension, active tobacco use, or diabetes mellitus also did not differ between the 2 groups (Table 1). Postbariatric patients lost an average of 151 lb and presented at an average of 32 months after gastric bypass. Diet-controlled weight loss patients lost an average of 124 lb before presentation. Despite MWL, albumin levels were higher in the gastric-bypass group (3.8 vs 3.4 g/dL, P G 0.05). Conversely, gastric-bypass patients experienced a significantly increased rate of wound complications (27% vs 14%, P G 0.05). Factors that were found to correlate with the increased risk of wound dehiscence and infection were elevated body mass index (BMI) at time of panniculectomy and volume of tissue removed. Ventral hernia was encountered and repaired in 15 (9%) patients, and was most commonly the result of a previous lower transverse incision. These hernias did not show a statistical relation to wound healing problems and there was no reported incidence of known recurrence in these 15 patients. Although more patients from the diet/exercise group did have a vertical component to the skin resection (38% vs 25%), this did not show an increased risk of wound healing despite the longer incision and wound closure. Multivariate analysis did not show serum albumin or percent weight loss to independently predict complications (Table 2).
DISCUSSION Despite the frequent improvement of medical comorbidities after MWL, previously obese patients are left with the stigmata of redundant skin. It is not surprising that the popularity of body contouring surgery has mirrored the rising trend of bariatric surgeries.3 Nearly, three quarters (74%) of postbariatric patients desire body-contouring surgery and abdominal contouring procedures including both panniculectomy and formal abdominoplasty are the most popular (59%).9 Unfortunately, body-contouring procedures are often associated with wound healing complications such as infection (16%Y48%), skin necrosis (6%Y10%), and wound dehiscence (13%Y33%).5 Although the number of patients presenting for body contouring after MWL continues to rise, there are no definitive guidelines on how to improve postsurgical outcomes. This
& Volume 75, Number 4, October 2015
TABLE 2. Preoperative Nutritional Comparison Between the Gastric Bypass and Nongastric Bypass Study Groups
Serum albumin, g/dL Serum prealbumin, mg/dL Hemoglobin level, mg/dL Serum iron, Hg/dL Serum calcium, mg/dL Serum glucose, mg/dL
Gastric Bypass (n = 124)
Nongastric Bypass (n = 37)
3.6 20.1 36.0 74 8.2 121
3.1* 14.7* 38.2 52 7.1 118
*Statistically significant difference at a P G 0.05.
study focused on the preoperative nutritional parameters and postsurgical complications of patients who underwent panniculectomy after MWL through either bariatric surgery or diet-controlled weight loss. It is worth noting that this is a retrospective analysis of 3 surgeon’s practices, with minor variances in patient selection and surgical techniques; however, multiple findings were consistent across each patient cohort. Despite increased serum protein markers, aggressive supplemental replacement and normalization of nutritional markers, the postbariatric group experienced increased rates of wound complications when compared to nonbariatric patients undergoing similar procedures (Figs. 1 and 2). A subgroup analysis of postbariatric patients did not show low albumin levels to be an accurate predictor of complications or reoperation. Two factors that were found to correlate with the increased risk of wound dehiscence and infection were elevated BMI at the time of panniculectomy and the amount of tissue removed. Multivariate analysis did not show serum albumin or percent weight loss to independently predict complications. Postbariatric patients frequently develop malnutrition given that the most common procedure, Roux-en-Y gastric bypass, combines both restrictive and malabsorptive aspects of bariatric surgery. Nutritional deficiency after bariatric surgery can be categorized into 3 types as follows: (1) vitamin/mineral deficiencies, (2) dehydration, and (3) protein-energy malnutrition.10 Among the vitamin and mineral deficiencies, iron deficiency after Roux-en-Y gastric bypass is especially common, as the usual sites of iron absorption, the duodenum and proximal jejunum, are no longer involved in the absorptive phase. Most germain to wound healing complications, though, is protein intolerance.
TABLE 1. Patient Demographics and Comparison of Associated Comorbidities
BMI, kg/m2 Age, y Time from surgery, mo Total weight loss, lb Weight of pannus removed, lb Active tobacco use, % Active diabetes, % Active hypertension, %
436
Gastric Bypass (n = 124)
Nongastric Bypass (n = 37)
33.8 42.6 32.1 142.1 24.1 8 37 10
36.4 40.5 V 124.2 19.7 10 44 9
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FIGURE 1. A 55-year-old woman underwent a 4650-g abdominal panniculectomy after diet-controlled weight loss. The superior vertical component was left open and negative pressure wound therapy was applied to decrease seroma formation. * 2014 Wolters Kluwer Health, Inc. All rights reserved.
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Annals of Plastic Surgery
& Volume 75, Number 4, October 2015
FIGURE 2. The same patient 9 days after abdominal panniculectomy, with complete dehiscence of her wound due to skin and fat necrosis. Of note, her albumin level was 3.3 g/dL before the initial operation.
In the absence of supplementation, protein malnutrition can develop.8 With rapid weight loss, the amino acid pool is diverted to gluconeogenesis, which, in combination with malabsorption and intolerance to high-protein foods, can lead to protein depletion.11 Protein deficiency inhibits maximal wound healing by impairing DNA production, neovascularization, fibroblast proliferation, collagen synthesis, and wound remodeling. Hypoproteinemia can also lead to decreased oxygenation and nutrient transport to the wound secondary to edema formation.12 Protein deficiency is traditionally recognized by low serum albumin, which indicates the depletion of total body proteins.13 Serum albumin concentrations of 3.5 g/dL or greater are considered normal; the values for mild, moderate, and severe depletion are 3.5Y2.8, 2.7Y2.1, and less than 2.1 g/dL, respectively.14 A plethora of published literature exists showing low serum albumin levels as a strong predictor for adverse surgical outcomes. A decrease in serum albumin from 4.6 to less than 2.1 g/dL is associated with an increase in postoperative sepsis and major infections.15 There are many studies that have stressed the importance of optimal nutrition before reconstructive surgery8,16Y18 and the utility of serum albumin levels, but our results indicate that there may not be a causative link between albumin levels and perioperative complications in MWL patients. Despite higher average albumin levels before surgery (3.8 vs 3.4 g/dL) and lower percent of albumin less than 3.5 g/dL (26% vs 50%), our bariatric patients had increased rates of wound complications after panniculectomy when compared to diet-controlled patients with lower albumin levels (WS, 27% vs 14%; WI, 26% vs 16%; P G 0.05). These findings correlate with those of Larson et al,19 who performed a 5-year retrospective chart review of 101 patients with 179 pressure ulcers, and unlinked patients’ preoperative nutritional status and investigated the rates of recurrence and complications. Neither admission prealbumin nor albumin levels were associated with 2-year recurrence or complications of pressure ulcers. Serum albumin and prealbumin levels were found to have significantly increased upon discharge and wound closure, indicating that large open wounds result in significant protein loss secondary to a chronic inf lammatory state. Due to the impracticality of admitting patients solely for nutritional supplementation and monitoring, they established a protocol with lower recurrence and complication rates of 16.8% and 17% compared to published rates of 12% to 82% and 16% to 46%.19 Specific factors which were found to correlate to increased risk of wound dehiscence and infection were elevated BMI at time of panniculectomy and volume of tissue removed. Previous associations between BMI, amount of tissue removed, and adverse outcomes are * 2014 Wolters Kluwer Health, Inc. All rights reserved.
Nutritional Markers in Wound Healing Complications
well documented.20Y22 A retrospective analysis by Vastine et al23 demonstrated an 80% complication rate for obese patients after abdominoplasty compared to the 33% and 32.5% for borderline obese and nonobese cohorts, respectively. Coon et al21 demonstrated in a prospective study of 449 bariatric patients undergoing body contouring that elevated BMI at the time of surgery was a predictor of complications. A retrospective study by Neaman and Hansen20 found a positive correlation between greater volumes of tissue removed and increased wound infections and dehiscence. With successful weight loss, a patient with a higher initial BMI who loses more weight is expected to have greater deformities requiring more extensive operations, which is ref lected in our study. Efforts to curtail complications and improve outcomes include perioperative attention to the medical comorbidities of the obese and MWL groups. Heart disease, hypertension, dyslipidemia, diabetes, obstructive sleep apnea, gastroesophageal reflux disease, and osteoarthritis are common comorbid conditions,24 generating increased postoperative complications of wound infections,25 pulmonary complications,26 thromboembolic events27 and increased mortality.28 The risk of surgical complications for associated morbidities seems to decrease as the patient’s BMI normalizes. Current best-practice recommendations include the delay of body-contouring surgery until the postbariatric or MWL patient has been weight stable for a period of 2 months, often corresponding to 12 to 18 months after gastric bypass.24 The best candidates for extensive body contouring have a BMI in the range of 25 to 30 kg/m2. This allows the patient to reach metabolic and nutritional homeostasis and better aesthetic outcomes upon reaching a stable weight.24 In our analysis, postbariatric patients presented at an average of 32 months after gastric bypass with a BMI of 33.8 kg/m2 and nongastric bypass patients with a higher BMI of 36.4 kg/m2. Both groups reached a stable maintenance weight before panniculectomy, yet the postbariatric group still had a greater rate of complications, even with a lower preoperative BMI. MWL patients do have significant nutritional deficiencies, and infraumbilical panniculectomy is known to have higher perioperative complication rates than other elective surgeries. We support that supplementation should be of benefit given evidence of the importance of protein in the wound healing process, but patients who are weightstable may still have tenuous protein and energy intake. Major elective surgery such as panniculectomy and abdominal contouring requires an increased energy and protein consumption of approximately 25%.29 Protein malnutrition in the bariatric population is difficult to diagnose and although the medical community has traditionally used serum albumin levels to reflect protein deficiency, current recommendations that have extrapolated a link between albumin levels and perioperative complications may be misleading.
CONCLUSIONS Despite being reported in the literature, associations between serum albumin and postoperative wound healing complications may not demonstrate a direct causative relationship. Variables that have increased predictive value for postoperative complications include an elevated BMI at time of surgery, as well as tissue resection volumes above 10 kg. Nutritional optimization should remain a cornerstone of appropriate perioperative management, however, patients with increased BMI or planned tissue resection volumes should be expectantly managed for postoperative wound healing complications. These data may provide increased evidence for staged resections with decreased wound tension or tissue trauma at the time of skin resection procedures. Accordingly, there is a need for further studies looking at other associated nutritional measures. In this way, patient outcomes can be optimized while minimizing avoidable surgical complications. REFERENCES 1. Trus TL, Pope GD, Finlayson SR. National trends in utilization and outcomes of bariatric surgery. Surg Endosc. 2005;19:616Y620.
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2. Ogden CCM, Kit BK, Flegal K. Centers for Disease Control and Prevention. Prevalence of Obesity in the United States, 2009-2010. 2009-2010. Accessed Accessed May 15, 2013. 3. Surgeons ASoP. Procedural Statistics, 2012. Available at: http://www.plasticsurgery.org/ Documents/news-resources/statistics/2012-Plastic-Surgery-Statistics/body-contouringafter-massive-weight-loss.pdf. Accessed May 15, 2013. 4. Greco JA 3rd, Castaldo ET, Nanney LB, et al. The effect of weight loss surgery and body mass index on wound complications after abdominal contouring operations. Ann Plast Surg. 2008;61:235Y242. 5. Acarturk TO, Wachtman G, Heil B, et al. Panniculectomy as an adjuvant to bariatric surgery. Ann Plast Surg. 2004;53:360Y366; discussion 367. 6. Naghshineh N, O’Brien Coon D, McTigue K, et al. Nutritional assessment of bariatric surgery patients presenting for plastic surgery: a prospective analysis. Plast Reconstr Surg. 2010;126:602Y610. 7. Russell L. The importance of patients’ nutritional status in wound healing. Br J Nurs. 2001;10(suppl 6):S42, S44YS49. 8. Agha-Mohammadi S, Hurwitz DJ. Enhanced recovery after body-contouring surgery: reducing surgical complication rates by optimizing nutrition. Aesthetic Plast Surg. 2010;34:617Y625. 9. Kitzinger HB, Abayev S, Pittermann A, et al. The prevalence of body contouring surgery after gastric bypass surgery. Obes Surg. 2012;22:8Y12. 10. Kaafarani HM, Shikora SA. Nutritional support of the obese and critically ill obese patient. Surg Clin North Am. 2011;91:837Y855, viii-ix. 11. Moize V, Geliebter A, Gluck ME, et al. Obese patients have inadequate protein intake related to protein intolerance up to 1 year following Roux-en-Y gastric bypass. Obes Surg. 2003;13:23Y28. 12. Hess CT. Monitoring laboratory values: protein and albumin. Adv Skin Wound Care. 2009;22:48. 13. Sebastian JL. Bariatric surgery and work-up of the massive weight loss patient. Clin Plast Surg. 2008;35:11Y26. 14. Grant JP, Custer PB, Thurlow J. Current techniques of nutritional assessment. Surg Clin North Am. 1981;61:437Y463. 15. Gibbs J, Cull W, Henderson W, et al. Preoperative serum albumin level as a predictor of operative mortality and morbidity: results from the National VA Surgical Risk Study. Arch Surg. 1999;134:36Y42.
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16. Araco A, Gravante G, Araco F, et al. Body contouring after weight loss: the plastic-bariatric surgery symbiosis. Aesthetic Plast Surg. 2006;30:374Y376. 17. Shermak MA, Chang D, Magnuson TH, et al. An outcomes analysis of patients undergoing body contouring surgery after massive weight loss. Plast Reconstr Surg. 2006;118:1026Y1031. 18. Ruberg RL. Role of nutrition in wound healing. Surg Clin North Am. 1984; 64:705Y714. 19. Larson DL, Hudak KA, Waring WP, et al. Protocol management of late-stage pressure ulcers: a 5-year retrospective study of 101 consecutive patients with 179 ulcers. Plast Reconstr Surg. 2012;129:897Y904. 20. Neaman KC, Hansen JE. Analysis of complications from abdominoplasty: a review of 206 cases at a university hospital. Ann Plast Surg. 2007;58:292Y298. 21. Coon D, Gusenoff JA, Kannan N, et al. Body mass and surgical complications in the postbariatric reconstructive patient: analysis of 511 cases. Ann Surg. 2009;249:397Y401. 22. Arthurs ZM, Cuadrado D, Sohn V, et al. Post-bariatric panniculectomy: prepanniculectomy body mass index impacts the complication profile. Am J Surg. 2007;193:567Y570; discussion 570. 23. Vastine VL, Morgan RF, Williams GS, et al. Wound complications of abdominoplasty in obese patients. Ann Plast Surg. 1999;42:34Y39. 24. Rubin JP, Toy J. Discussion. Prospective assessment of nutrition and exercise parameters before body contouring surgery: optimizing attainability in the massive weight loss population. Plast Reconstr Surg. 2010;125:1248Y1249. 25. Thomas EJ, Goldman L, Mangione CM, et al. Body mass index as a correlate of postoperative complications and resource utilization. Am J Med. 1997;102: 277Y283. 26. Gould AB Jr. Effect of obesity on respiratory complications following general anesthesia. Anesth Analg. 1962;41:448Y452. 27. Colwell CW Jr, Collis DK, Paulson R, et al. Comparison of enoxaparin and warfarin for the prevention of venous thromboembolic disease after total hip arthroplasty. Evaluation during hospitalization and three months after discharge. J Bone Joint Surg Am. 1999;81:932Y940. 28. Prem KA, Mensheha N, McKelvey JL. Operative treatment of adenocarcinoma of the endometrium in obese women. Am J Obstet Gynecol. 1965;92:16Y22. 29. Van Way CW 3rd. Nutritional support in the injured patient. Surg Clin North Am. 1991;71:537Y548.
* 2014 Wolters Kluwer Health, Inc. All rights reserved.
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