ORIGINAL ARTICLE
The Effect of Body Mass Index on Postoperative Morbidity After Orthopaedic Surgery in Children With Cerebral Palsy Shobhit V. Minhas, BA,* Ian Chow, BA,* and Norman Y. Otsuka, MDw
Background: Although a plethora of literature exists on the impact of body mass index (BMI) in orthopaedic surgery, few have examined its implications in the pediatric cerebral palsy (CP) population. The aim of this study is to evaluate the effect of BMI class on 30-day complications after orthopaedic surgery on children with CP. Methods: A retrospective analysis of the American College of Surgeons National Surgical Quality Improvement Program (NSQIP) Pediatric participant use files from 2012 to 2013 was conducted. Patients with a diagnosis of CP undergoing any orthopaedic procedure were included and subclassified according to BMI classes: underweight, normal weight, overweight, and obese. Multivariate logistic regressions were performed to evaluate the independent effect of BMI class on total, surgical site, and medical complications as well as unplanned reoperations. Results: A total of 1746 patients were included in our study. These included 345 (19.8%) underweight, 952 (54.5%) normal weight, 209 (12.8%) overweight, and 240 (13.7%) obese children and adolescents. In hip and lower extremity osteotomies, underweight class was an independent risk factor for total complications (P = 0.037) and medical complications (P = 0.031). Similarly, underweight class was a risk factor for total complications (P = 0.022) and medical complications (P = 0.019) in spine procedures. Weight class was not independently associated with complications in tendon procedures. Overweight and obesity classes were not associated with any independent increased risk for complications. Conclusions: With respect to the pediatric CP population, underweight status was deemed an independent predictor of increased complications in osteotomies and spine surgery with no independent increased risk in the overweight or obese cohorts. This information can greatly aid providers with risk stratification, preoperative counseling, and postoperative monitoring as it relates to orthopaedic surgery. Level of Evidence: Level III—Prognostic. From the *Ann & Robert H. Lurie Children’s Hospital of Chicago, Northwestern University, Feinberg School of Medicine, Chicago, IL; and wCenter for Children, NYU Hospital for Joint Diseases, New York, NY. The authors disclose that they have not received any outside source of funding for any portion of this study. The authors declare no conflicts of interest. Reprints: Shobhit V. Minhas, BA, 441 East Erie Street, Apt 2713, Chicago, IL 60611. E-mail: [email protected]. Supplemental Digital Content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Website, www. pedorthopaedics.com. Copyright r 2015 Wolters Kluwer Health, Inc. All rights reserved.
J Pediatr Orthop
Volume 36, Number 5, July/August 2016
Key Words: cerebral palsy, BMI, complications, obesity, malnutrition, NSQIP (J Pediatr Orthop 2016;36:505–510)
C
erebral palsy (CP) is a heterogenous collection of nonprogressive disorders of movement and posture, often escorted by disturbances in cognition, sensation, and behavior.1 CP is the leading cause of childhood disability, with a reported incidence of 2 to 3 in 1000 live births and a stable to slightly increasing prevalence in the last few decades.2 Appropriate interventions for CP are decreed by the patient’s disease severity, functional ability, pain, and quality of life, and often require surgical mediation. These children are particularly at risk for hip subluxation, rapidly progressive scoliosis, and extensive contraction formation, subsequently requiring the need for orthopaedic surgery.3,4 Although orthopaedic procedures have shown to provide excellent results in terms of deformity and motor function in the pediatric CP population, postoperative morbidity is high.3,5 One explanation is the pervasiveness of poor nutrition and hence growth restriction and underweight status in these patients, which increases the risk for immunity dysfunction, poor wound healing, and immobility.6–8 Although malnutrition and underweight is common, the prevalence of obesity in children with CP has also dramatically increased over the last decade, particularly in ambulatory patients.9 Obesity not only is associated with a myriad of health problems, but also is a strong contributor to postoperative morbidity after pediatric surgery. Although an extensive focus has been on body mass index (BMI) in orthopaedic literature, we are unaware of any large, multicentered study that has examined the effect of this metric on complications in the pediatric CP population. In this study, we aim to evaluate the effect of BMI on 30-day complications after pediatric orthopaedic procedures on patients with CP through the American College of Surgeons (ACS) National Surgical Quality Improvement Program (NSQIP) Pediatric database. This national, multicentered prospective database has been frequently utilized to analyze trends in pediatric surgery.10,11 The specific aims of this study are to (1) establish a baseline prevalence of weight classifications on the basis of BMI in children with CP undergoing orthopaedic surgery, and (2) to examine the independent effect of BMI on 30-day postoperative complications with respect to orthopaedics. www.pedorthopaedics.com |
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METHODS Data Source A retrospective analysis of 2012 to 2013 ACSNSQIP Pediatric participant use files was conducted. The distinct advantage of using this database over others is the large variety of variables (129 total demographics, comorbidities, operative characteristics, and 30-d complications), the inclusion of postdischarge events as well as in-house complications, the inclusion of >50 institutions throughout the country, and the low rate of interobserver disagreement rate (< 5% as per the pediatric NSQIP participant user file). As per its user guidelines, patient variables are de-identified to comply with the Health Insurance Portability and Accountability Act (HIPAA) of 1996 and do not require Institutional Review Board approval. Detailed descriptions of the methodologies of data collection from the NSQIP database has been described in detail.12
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lignancy, preoperative inotrope requirement, prior operation within last 30 days, preoperative transfusion requirement, and American Society of Anesthesiologists (ASA) Class Z3. Thirty-day complications consisted of wound complications, medical complications, unplanned reoperations, and mortality. Wound complications included superficial surgical site infections, deep surgical site infections, organ space infections, and wound disruptions. Medical complications comprised respiratory (pneumonia and reintubation), thromboembolic (pulmonary embolus and venous clot), renal (renal insufficiency, acute renal failure, and urinary tract infections), neurological (coma, cerebrovascular event, seizure, nerve injury, and intraventricular hemorrhage), cardiac (cardiac arrest), bleeding, and infectious (sepsis and central line infection) complications.
Statistical Analysis Patient Selection and Comparison of Cohorts All patients undergoing orthopaedic surgery with a diagnosis of CP undergoing: (1) hip, femoral, and tibial osteototomy, (2) spine, and (3) tendon procedures by Current Procedural Terminology (CPT) codes (defined by the American Medical Association) were selected from the NSQIP database. A detailed listing of procedures is shown in Appendix 1 (Supplemental Digital Content, http://links.lww.com/BPO/A35). Per the NSQIP participant use file, patients with CP were defined as “patients who have been diagnosed with CP with associated motor and/or cognitive deficits due to known or unknown etiology.” All patients with missing height and/or weight values and of less than 2 years of age were excluded. After being divided into their 3 respective procedure cohorts (spine, tendon, and hip and lower extremity osteotomy), patients were stratified into groups on the basis of weight classification as per the Centers for Disease Control and Prevention: underweight (BMI < fifth percentile by age), normal weight (fifth percentilerBMI < 85th percentile by age), overweight (85th percentilerBMI < 95th percentile by age), and obese (BMIZ95th percentile by age). Demographics, comorbidities, and 30-day complications were compared between the 4 weight stratifications for each procedure group. Patient demographics and comorbidities included age, sex, diabetes, premature birth, ventilator requirement, asthma, cystic fibrosis, chronic lung disease, oxygen requirement, tracheostomy, structural pulmonary abnormality, esophageal or gastrointestinal disease, hepatobiliary or pancreatic disease, cardiac risk factors, dialysis requirement, history of cerebrovascular event, central nervous system tumor, history of seizure, structural central nervous system abnormality, history of intraventricular hemorrhage, immunity disorder, chronic steroid use, nutritional support through total parenteral nutrition or feeding tubes, bone marrow disorder, history of organ transplant, open wound, bleeding disorder, hematological disorder, history of chemotherapy, history of radiotherapy, childhood ma-
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IBM SPSS Version 22 (Chicago, IL) was used for all descriptive and comparative analyses. In all cases, Pr0.05 was defined as statistically significant. Univariate analysis using the Pearson w2 test was used to compare preoperative demographics and comorbidities between the underweight, normal weight, overweight, and obese cohorts. In addition, univariate analysis of the CPT code was also used to assess for potential procedural discrepancies between weight classes. Multivariate regression analyses were then performed to determine the independent association of BMI classification on total complications, wound complications, medical complications, and unplanned reoperations for each of the 3 procedure groupings. In cases in which too few complications occurred for adequate multivariate models, regression analyses were not conducted. In all multivariate analyses, an operative procedure based on the CPT code was included in order to extrapolate the independent effects of BMI class regardless of orthopaedic intervention. Normal weight class was set as the reference. Candidate variables for our multivariate analyses were identified and screened from which only variables with P < 0.2 and >5 complication incidences from univariate analyses of preoperative variables on complications.13 Hosmer-Lemeshow and c-statistics were calculated to assess the calibration and goodness-of-fit of the model, respectively, for each regression.14
RESULTS Patient Characteristics A total of 1746 patients were included in our study. Overall, these included 345 (19.8%) underweight, 952 (54.5%) normal weight, 209 (12.0%) overweight, and 240 (13.7%) obese children and adolescents. Specific weight class proportions based on the procedural group are indicated in Table 1 along with those preoperative variables showing significant rate discrepancies among the 4 weight groups, described below. Copyright
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J Pediatr Orthop
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BMI in Cerebral Palsy
Univariate Comparison of Demographics, Comorbidities, and Complications Table 1 contains a detailed list of those preoperative variables that significantly differed among weight classes for each procedural cohort. No other significant differences in preoperative variables existed among weight classes in any of the 3 procedural groups, including CPT codes (P = 0.061 to 0.374). In addition, 32.7% (osteotomies), 47.9% (spine), and 13.9% (tendon procedures) of underweight patients were receiving preoperative nutritional support with no significant differences in nutritional support among weight classes. Underweight CP patients had higher rates of sepsis (P = 0.003) in the osteotomy group and higher rates of bleeding in the spine surgery group (P = 0.025). In the spine cohort, obese patients had higher rates of wound disruption (P = 0.045) with no differences in complication rates in our univariate analysis in the tendon procedure group.
Multivariate Analyses With respect to osteotomy procedures, underweight class was an independent risk factor for developing any postoperative complication [odds ratio (OR) 1.72, 95% confidence interval (CI): 1.03-2.86, P = 0.037] and medical complication (OR 1.80, CI: 1.06-3.06, P = 0.031), whereas overweight class and obesity were not associated with any independent increased risk of any complication, any medical complication, or wound complications (Table 2). Similarly, underweight was associated with an increased risk of total complications (OR 1.99, CI: 1.11-3.59, P = 0.022) and medical complications (OR 1.95, CI: 1.12-3.41, P = 0.019) in the spine surgery cohort (Table 3). Finally, weight class was not independently associated with total complications or surgical site complications in CP patients receiving tendon procedures (Table 4). Multivariate analyses were not conducted on medical complications in the tendon surgery group or reoperations in the tendon surgery and osteotomy
group due to low 30-day incidences in those cohorts. Our c indices of 0.703-0.934 represented excellent predictive models.
DISCUSSION BMI in the pediatric population is an age-adjusted anthropometric measure used to appropriately assess growth development, nutritional status, and comorbidity burden.15 Underweight and obesity are extreme weight percentiles, and have been corroborated as risk factors for postsurgical morbidity and mortality. Underweight is a measure of malnutrition, which has been associated with increased risk of infections, numerous medical complications, and death in surgical patients.16–18 The nutritional demands of children in appropriate wound healing and recovery after operative intervention are fundamental in preventing short-term complications. Concurrently, obesity in children has been linked to surgical site infections, thromboembolic events, and decubitus ulcers.19,20 Obesity can involve thick subcutaneous adipose layers, which can form dead space after closure, increasing the risk for site infection and wound disruption through necrosis of local fat.21 Obesity has also been linked to numerous other comorbidities, which lends itself to poor postoperative courses. Alarmingly, the national rate of obesity has precipitously grown in the last few decades, with an associated increased incidence in children with CP.9 In our study of children and adolescents with CP undergoing orthopaedic procedures, the prevalence of underweight and obesity were 19.8% and 13.7%, respectively, similar to rates shown in previous literature.9 Our results demonstrate that underweight CP patients are independently at risk for 30-day postoperative complications after orthopaedic surgery, particularly medical complications, for both spine procedures and osteotomies. BMI class in tendon procedures, likely due to the low overall complication rate, did not affect morbidity and mortality. Univariate analysis demonstrated the
TABLE 1. Statistically Significant Discrepancies in Patient Demographics and Comorbidities Based on Weight Classification Patient Characteristic
Underweight [n (%)]
Hip or lower extremity osteotomy procedure (n = 467) n 104 Diabetes 0 (0.00) Asthma 12 (11.54) Chronic steroid use 1 (0.96) Spine procedure (n = 468) n 140 Diabetes 1 (0.71) Ventilator requirement 8 (5.71) Tracheostomy 4 (2.86) Tendon procedure (n = 811) n 101 Asthma 3 (2.97) CNS tumor 0 (0.00) Seizure disorder 32 (31.68) Chronic steroid use 1 (0.99) ASAZ3 53 (52.48)
P
Normal Weight [n (%)]
Overweight [n (%)]
Obese [n (%)]
247 0 (0.00) 27 (10.93) 1 (0.40)
51 0 (0.00) 13 (25.49) 1 (1.96)
65 2 (3.08) 15 (23.08) 5 (7.69)
0.006 0.007 0.021
241 1 (0.41) 14 (5.81) 17 (7.05)
44 0 (0.00) 8 (18.18) 7 (15.91)
43 2 (4.65) 3 (6.98) 4 (9.30)
0.041 0.026 0.022
39 0 87 0 132
464 (8.41) (0.00) (18.75) (0.00) (28.45)
9 0 21 0 34
114 (7.89) (0.00) (18.42) (0.00) (29.82)
14 2 31 3 38
132 (10.61) (1.52) (23.48) (2.27) (28.79)
0.021 0.016 0.026 0.008 < 0.001
ASA indicates American Society of Anesthesiologists; CNS, central nervous system.
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TABLE 2. Multivariate Analysis of Weight Classification on Complications in Hip or Lower Extremity Osteotomies (n = 467) 95% CI Weight Category Any complication Underweight Normal weight Overweight Obese Any surgical site complication Underweight Normal weight Overweight Obese Any medical complication Underweight Normal weight Overweight Obese
Odds Ratio
Lower
Upper
P
Hosmer-Lemeshow
c Statistic
1.72 REF 0.72 0.68
1.03 REF 0.33 0.32
2.86 REF 1.56 1.42
0.037* REF 0.397 0.302
0.316
0.730
1.77 REF 3.87 1.89
0.30 REF 0.50 0.14
10.36 REF 12.24 16.00
0.528 REF 0.196 0.635
0.907
0.926
1.80 REF 0.64 0.79
1.06 REF 0.28 0.36
3.06 REF 1.46 1.71
0.031* REF 0.290 0.310
0.153
0.763
*Significant value (Pr0.05). CI indicates confidence interval; REF, reference value.
highest rates of both postoperative bleeding requiring transfusion in spine surgery and sepsis in osteotomies in the underweight. Malnutrition is often associated with iron deficiency anemia, and hence may account for the postoperative transfusion requirement.22 Although it is possible that underweight patients underwent more extensive procedures, after stratification through procedures, no significant differences in CPT codes existed between weight classes. Malnutrition is also associated with impaired gut barrier function, low levels of complement, atrophied lymphatic tissue, reduced exocrine protective factors, and other immunologic aberrations, which place these patients at increased risk for systemic
infections.23 In addition, it has been shown that patients with more involved CP and higher Gross Motor Function Classification System (GMFCS) scores, and hence more involved surgical intervention, are also at a higher risk for malnutrition.8 Whereas low BMI was an independent risk factor for postoperative morbidity in CP patients, to our surprise, obesity was not, although higher rates of wound dehiscence were seen in obese patients after spine procedures. In pediatric orthopaedic surgery, although the impact of obesity on complications has been limited, the majority of studies demonstrate a strong association mostly with respect to long-term complication, not assessed with our data.24–28 It
TABLE 3. Multivariate Analysis of Weight Classification on Complications in Spine Procedures (n = 468) 95% CI Weight Category Any complication Underweight Normal weight Overweight Obese Any surgical site complication Underweight Normal weight Overweight Obese Any medical complication Underweight Normal Weight Overweight Obese Any unplanned reoperation Underweight Normal weight Overweight Obese
Odds Ratio
Lower
Upper
P
Hosmer-Lemeshow
c Statistic
1.99 REF 0.67 0.88
1.11 REF 0.31 0.4
3.59 REF 1.45 1.98
0.022* REF 0.31 0.762
0.240
0.739
0.50 REF 0.74 0.55
0.20 REF 0.16 0.12
1.28 REF 3.49 2.59
0.148 REF 0.704 0.453
0.354
0.763
1.95 REF 0.56 0.85
1.12 REF 0.26 0.38
3.41 REF 1.22 1.89
0.019* REF 0.145 0.689
0.126
0.703
0.53 REF 0.17 1.38
0.24 REF 0.02 0.51
1.17 REF 1.31 3.76
0.117 REF 0.088 0.530
0.384
0.726
*Significant value (Pr0.05). CI indicates confidence interval; REF, reference value.
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J Pediatr Orthop
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BMI in Cerebral Palsy
TABLE 4. Multivariate Analysis of Weight Classification on Complications in Tendon Procedures (n = 811) 95% CI Weight Category Any complication Underweight Normal weight Overweight Obese Any surgical site complication Underweight Normal weight Overweight Obese
Odds Ratio
Lower
Upper
P
Hosmer-Lemeshow
c Statistic
1.60 REF 0.44 0.20
0.32 REF 0.05 0.01
7.93 REF 4.33 3.77
0.563 REF 0.485 0.283
0.632
0.934
0.55 REF 0.76 1.08
0.06 REF 0.08 0.12
5.41 REF 6.99 10.19
0.610 REF 0.806 0.946
0.932
0.830
CI indicates confidence interval; REF, reference value.
is unclear why obese and overweight patients in our cohort do not have an increased risk of postoperative morbidity. One hypothesis is that obese patients may have less involved CP and increased functional status, which may play a potential protective role to offset the risk of adverse events typically associated with increasing body mass. Another conjecture is that the unaffected nutritional status in obese patients when compared with normal-weight patients supersedes the deleterious effects of elevated BMI. This implication endorses the importance of preoperative nutritional status with respect to risk stratification—namely that underweight CP children have an increased risk for complications, and hence require more extensive preoperative evaluation, risk counseling for parents, and postoperative care and monitoring. Fortunately, preoperative malnutrition is often subject to modification and improvement. Interestingly, although underweight patients had higher complications in spinal surgery and osteotomies, less than half of those patients were receiving preoperative nutritional support, and rates of nutritional support did not significantly vary among weight classes for any of our 3 procedure groups. Several studies have examined the role of postoperative nutritional supplementation, which have been shown to decrease rates of infection and hospital length of stay following orthopaedic procedures.29 Hence, more aggressive attempts to address nutritional status with specific preoperative nutrition plans in the underweight group before osteotomies and spinal intervention may improve outcomes. This study is not without limitations. First is the fact that the ACS-NSQIP pediatric database does not include information regarding the severity of CP or markers of functional status, such as the Gross Motor Function Classification System (GMFCS) score, and, although it includes nutritional support as a variable, it does not indicate poor nutritional status as many patients with this comorbidity may not be on supplementation. Functional and ambulatory status may be a confounder in our analysis of BMI and complication rates, and may be potentially responsible for the surprising result that obesity does not contribute to an increased risk for perioperative adverse events. This database also does not include geographic information, pediatric orthopaedic surgeon experience, and academic versus private Copyright
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hospital type—all of which may also be potential confounders. Furthermore, although the list of preoperative confounding comorbidities in our study is fairly extensive, there may be others not included in NSQIP that we were not able to control for. In addition, the 30-day window is an intrinsic limitation in our study, as complications can occur outside of this time interval. It is possible that certain weight classes such as obesity may have more long-term complications that cannot be evaluated with our data set. Specifically, our analysis does not shed light on a number of long-term complications, such as malunion, failure of hardware, cast complications, pain, and poor functional improvement, all of which have been associated in the obese pediatric population. Hence, readers must be mindful that our data do not demonstrate overall postoperative differences, but provides a commentary regarding disparities in short-term perioperative events between weight classes. Our results reveal certain complications that practitioners should be mindful of in the immediate postoperative period, which has implications for 30-day follow-up, surveillance, and management.
CONCLUSIONS We present a comprehensive evaluation of the effect of BMI on 30-day complications after pediatric orthopaedic surgery on patients with CP. To our knowledge, this is the largest and first national, multicentered analysis of weight classification and postoperative morbidity and mortality in the pediatric CP population. Underweight status was deemed an independent predictor of increased 30-day complications in certain procedures. This information can greatly aid providers with risk stratification, preoperative counseling, and postoperative monitoring as it relates to orthopaedic surgery. REFERENCES 1. Bax M, Goldstein M, Rosenbaum P, et al. Proposed definition and classification of cerebral palsy, April 2005. Dev Med Child Neurol. 2005;47:571–576. 2. Colver A, Fairhurst C, Pharoah PO. Cerebral palsy. Lancet. 2014;383:1240–1249. 3. Sponseller PD, Shah SA, Abel MF, et al. Infection rate after spine surgery in cerebral palsy is high and impairs results: multicenter analysis of risk factors and treatment. Clin Orthop Relat Res. 2010;468:711–716.
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4. Firth GB, Passmore E, Sangeux M, et al. Multilevel surgery for equinus gait in children with spastic diplegic cerebral palsy: mediumterm follow-up with gait analysis. J Bone Joint Surg Am. 2013;95: 931–938. 5. Mohamed Ali MH, Koutharawu DN, Miller F, et al. Operative and clinical markers of deep wound infection after spine fusion in children with cerebral palsy. J Pediatr Orthop. 2010;30:851–857. 6. Kuperminc MN, Stevenson RD. Growth and nutrition disorders in children with cerebral palsy. Dev Disabil Res Rev. 2008;14:137–146. 7. Chandra RK, Kumari S. Nutrition and immunity: an overview. J Nutr. 1994;124:1433s–1435s. 8. Feeley BT, Gollapudi K, Otsuka NY. Body mass index in ambulatory cerebral palsy patients. J Pediatr Orthop B. 2007; 16:165–169. 9. Rogozinski BM, Davids JR, Davis RB, et al. Prevalence of obesity in ambulatory children with cerebral palsy. J Bone Joint Surg Am. 2007;89:2421–2426. 10. Tahiri Y, Fischer JP, Wink JD, et al. Analysis of risk factors associated with 30-day readmissions following pediatric plastic surgery - a review of 5,376 procedures. Plast Reconstr Surg. 2014;2: 521–529. 11. Shah RK, Stey AM, Jatana KR, et al. Identification of opportunities for quality improvement and outcome measurement in pediatric otolaryngology. JAMA Otolaryngol Head Neck Surg. 2014;11:1019–1026. 12. Birkmeyer JD, Shahian DM, Dimick JB, et al. Blueprint for a new American College of Surgeons: National Surgical Quality Improvement Program. J Am Coll Surg. 2008;207:777–782. 13. Peduzzi P, Concato J, Kemper E, et al. A simulation study of the number of events per variable in logistic regression analysis. J Clin Epidemiol. 1996;49:1373–1379. 14. Merkow RP, Bilimoria KY, Hall BL. Interpretation of the Cstatistic in the context of ACS-NSQIP models. Ann Surg Oncol. 2011;18(suppl 3):S295–S296. 15. Lacher M, Froehlich S, von Schweinitz D, et al. Early and long term outcome in children with esophageal atresia treated over the last 22 years. Klin Padiatr. 2010;222:296–301. 16. Fu MC, Buerba RA, Grauer JN. Preoperative nutritional status as an adjunct predictor of major postoperative complications following
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anterior cervical discectomy and fusion. J Spinal Disord Tech. 2014. [Epub ahead of print]. O’Daly BJ, Walsh JC, Quinlan JF, et al. Serum albumin and total lymphocyte count as predictors of outcome in hip fractures. Clin Nutr. 2010;29:89–93. Koval KJ, Maurer SG, Su ET, et al. The effects of nutritional status on outcome after hip fracture. J Orthop Trauma. 1999;13:164–169. Rana AR, Michalsky MP, Teich S, et al. Childhood obesity: a risk factor for injuries observed at a level-1 trauma center. J Pediatr Surg. 2009;44:1601–1605. Brown CV, Neville AL, Salim A, et al. The impact of obesity on severely injured children and adolescents. J Pediatr Surg. 2006;41: 88–91; discussion 88-91. Mehta AI, Babu R, Karikari IO, et al. 2012 Young Investigator Award winner: the distribution of body mass as a significant risk factor for lumbar spinal fusion postoperative infections. Spine. 2012;37:1652–1656. Domellof M, Braegger C, Campoy C, et al. Iron requirements of infants and toddlers. J Pediatr Gastroenterol Nutr. 2014;58:119–129. Rytter MJ, Kolte L, Briend A, et al. The immune system in children with malnutrition—a systematic review. PloS one. 2014;9:e105017. Fedorak GT, Cuomo AV, Otsuka NY. Does pediatric body mass index affect surgical outcomes of lower-extremity external fixation? J Pediatr Orthop. 2014. [Epub ahead of print]. Burghardt RD, Specht SC, Herzenberg JE. Mechanical failures of eight-plateguided growth system for temporary hemiepiphysiodesis. J Pediatr Orthop. 2010;30:594–597. Linam WM, Margolis PA, Staat MA, et al. Risk factors associated with surgical site infection after pediatric posterior spinal fusion procedure. Infect Control Hosp Epidemiol. 2009;30:109–116. Leet AI, Pichard CP, Ain MC. Surgical treatment of femoral fractures in obese children: does excessive body weight increase the rate of complications? J Bone Joint Surg Am. 2005;87:2609–2613. Weiss JM, Choi P, Ghatan C, et al. Complications with flexible nailing of femur fractures more than double with child obesity and weight > 50 kg. J Child Orthop. 2009;3:53–58. Lawson RM, Doshi MK, Barton JR, et al. The effect of unselected post-operative nutritional supplementation on nutritional status and clinical outcome of orthopaedic patients. Clin Nutr. 2003;22:39–46.
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The Effect of Body Mass Index on Postoperative Morbidity After Orthopaedic Surgery in Children With Cerebral Palsy Shobhit V. Minhas, BA,* Ian Chow, BA,* and Norman Y. Otsuka, MDw
Background: Although a plethora of literature exists on the impact of body mass index (BMI) in orthopaedic surgery, few have examined its implications in the pediatric cerebral palsy (CP) population. The aim of this study is to evaluate the effect of BMI class on 30-day complications after orthopaedic surgery on children with CP. Methods: A retrospective analysis of the American College of Surgeons National Surgical Quality Improvement Program (NSQIP) Pediatric participant use files from 2012 to 2013 was conducted. Patients with a diagnosis of CP undergoing any orthopaedic procedure were included and subclassified according to BMI classes: underweight, normal weight, overweight, and obese. Multivariate logistic regressions were performed to evaluate the independent effect of BMI class on total, surgical site, and medical complications as well as unplanned reoperations. Results: A total of 1746 patients were included in our study. These included 345 (19.8%) underweight, 952 (54.5%) normal weight, 209 (12.8%) overweight, and 240 (13.7%) obese children and adolescents. In hip and lower extremity osteotomies, underweight class was an independent risk factor for total complications (P = 0.037) and medical complications (P = 0.031). Similarly, underweight class was a risk factor for total complications (P = 0.022) and medical complications (P = 0.019) in spine procedures. Weight class was not independently associated with complications in tendon procedures. Overweight and obesity classes were not associated with any independent increased risk for complications. Conclusions: With respect to the pediatric CP population, underweight status was deemed an independent predictor of increased complications in osteotomies and spine surgery with no independent increased risk in the overweight or obese cohorts. This information can greatly aid providers with risk stratification, preoperative counseling, and postoperative monitoring as it relates to orthopaedic surgery. Level of Evidence: Level III—Prognostic. From the *Ann & Robert H. Lurie Children’s Hospital of Chicago, Northwestern University, Feinberg School of Medicine, Chicago, IL; and wCenter for Children, NYU Hospital for Joint Diseases, New York, NY. The authors disclose that they have not received any outside source of funding for any portion of this study. The authors declare no conflicts of interest. Reprints: Shobhit V. Minhas, BA, 441 East Erie Street, Apt 2713, Chicago, IL 60611. E-mail: [email protected]. Supplemental Digital Content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Website, www. pedorthopaedics.com. Copyright r 2015 Wolters Kluwer Health, Inc. All rights reserved.
J Pediatr Orthop
Volume 36, Number 5, July/August 2016
Key Words: cerebral palsy, BMI, complications, obesity, malnutrition, NSQIP (J Pediatr Orthop 2016;36:505–510)
C
erebral palsy (CP) is a heterogenous collection of nonprogressive disorders of movement and posture, often escorted by disturbances in cognition, sensation, and behavior.1 CP is the leading cause of childhood disability, with a reported incidence of 2 to 3 in 1000 live births and a stable to slightly increasing prevalence in the last few decades.2 Appropriate interventions for CP are decreed by the patient’s disease severity, functional ability, pain, and quality of life, and often require surgical mediation. These children are particularly at risk for hip subluxation, rapidly progressive scoliosis, and extensive contraction formation, subsequently requiring the need for orthopaedic surgery.3,4 Although orthopaedic procedures have shown to provide excellent results in terms of deformity and motor function in the pediatric CP population, postoperative morbidity is high.3,5 One explanation is the pervasiveness of poor nutrition and hence growth restriction and underweight status in these patients, which increases the risk for immunity dysfunction, poor wound healing, and immobility.6–8 Although malnutrition and underweight is common, the prevalence of obesity in children with CP has also dramatically increased over the last decade, particularly in ambulatory patients.9 Obesity not only is associated with a myriad of health problems, but also is a strong contributor to postoperative morbidity after pediatric surgery. Although an extensive focus has been on body mass index (BMI) in orthopaedic literature, we are unaware of any large, multicentered study that has examined the effect of this metric on complications in the pediatric CP population. In this study, we aim to evaluate the effect of BMI on 30-day complications after pediatric orthopaedic procedures on patients with CP through the American College of Surgeons (ACS) National Surgical Quality Improvement Program (NSQIP) Pediatric database. This national, multicentered prospective database has been frequently utilized to analyze trends in pediatric surgery.10,11 The specific aims of this study are to (1) establish a baseline prevalence of weight classifications on the basis of BMI in children with CP undergoing orthopaedic surgery, and (2) to examine the independent effect of BMI on 30-day postoperative complications with respect to orthopaedics. www.pedorthopaedics.com |
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METHODS Data Source A retrospective analysis of 2012 to 2013 ACSNSQIP Pediatric participant use files was conducted. The distinct advantage of using this database over others is the large variety of variables (129 total demographics, comorbidities, operative characteristics, and 30-d complications), the inclusion of postdischarge events as well as in-house complications, the inclusion of >50 institutions throughout the country, and the low rate of interobserver disagreement rate (< 5% as per the pediatric NSQIP participant user file). As per its user guidelines, patient variables are de-identified to comply with the Health Insurance Portability and Accountability Act (HIPAA) of 1996 and do not require Institutional Review Board approval. Detailed descriptions of the methodologies of data collection from the NSQIP database has been described in detail.12
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lignancy, preoperative inotrope requirement, prior operation within last 30 days, preoperative transfusion requirement, and American Society of Anesthesiologists (ASA) Class Z3. Thirty-day complications consisted of wound complications, medical complications, unplanned reoperations, and mortality. Wound complications included superficial surgical site infections, deep surgical site infections, organ space infections, and wound disruptions. Medical complications comprised respiratory (pneumonia and reintubation), thromboembolic (pulmonary embolus and venous clot), renal (renal insufficiency, acute renal failure, and urinary tract infections), neurological (coma, cerebrovascular event, seizure, nerve injury, and intraventricular hemorrhage), cardiac (cardiac arrest), bleeding, and infectious (sepsis and central line infection) complications.
Statistical Analysis Patient Selection and Comparison of Cohorts All patients undergoing orthopaedic surgery with a diagnosis of CP undergoing: (1) hip, femoral, and tibial osteototomy, (2) spine, and (3) tendon procedures by Current Procedural Terminology (CPT) codes (defined by the American Medical Association) were selected from the NSQIP database. A detailed listing of procedures is shown in Appendix 1 (Supplemental Digital Content, http://links.lww.com/BPO/A35). Per the NSQIP participant use file, patients with CP were defined as “patients who have been diagnosed with CP with associated motor and/or cognitive deficits due to known or unknown etiology.” All patients with missing height and/or weight values and of less than 2 years of age were excluded. After being divided into their 3 respective procedure cohorts (spine, tendon, and hip and lower extremity osteotomy), patients were stratified into groups on the basis of weight classification as per the Centers for Disease Control and Prevention: underweight (BMI < fifth percentile by age), normal weight (fifth percentilerBMI < 85th percentile by age), overweight (85th percentilerBMI < 95th percentile by age), and obese (BMIZ95th percentile by age). Demographics, comorbidities, and 30-day complications were compared between the 4 weight stratifications for each procedure group. Patient demographics and comorbidities included age, sex, diabetes, premature birth, ventilator requirement, asthma, cystic fibrosis, chronic lung disease, oxygen requirement, tracheostomy, structural pulmonary abnormality, esophageal or gastrointestinal disease, hepatobiliary or pancreatic disease, cardiac risk factors, dialysis requirement, history of cerebrovascular event, central nervous system tumor, history of seizure, structural central nervous system abnormality, history of intraventricular hemorrhage, immunity disorder, chronic steroid use, nutritional support through total parenteral nutrition or feeding tubes, bone marrow disorder, history of organ transplant, open wound, bleeding disorder, hematological disorder, history of chemotherapy, history of radiotherapy, childhood ma-
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IBM SPSS Version 22 (Chicago, IL) was used for all descriptive and comparative analyses. In all cases, Pr0.05 was defined as statistically significant. Univariate analysis using the Pearson w2 test was used to compare preoperative demographics and comorbidities between the underweight, normal weight, overweight, and obese cohorts. In addition, univariate analysis of the CPT code was also used to assess for potential procedural discrepancies between weight classes. Multivariate regression analyses were then performed to determine the independent association of BMI classification on total complications, wound complications, medical complications, and unplanned reoperations for each of the 3 procedure groupings. In cases in which too few complications occurred for adequate multivariate models, regression analyses were not conducted. In all multivariate analyses, an operative procedure based on the CPT code was included in order to extrapolate the independent effects of BMI class regardless of orthopaedic intervention. Normal weight class was set as the reference. Candidate variables for our multivariate analyses were identified and screened from which only variables with P < 0.2 and >5 complication incidences from univariate analyses of preoperative variables on complications.13 Hosmer-Lemeshow and c-statistics were calculated to assess the calibration and goodness-of-fit of the model, respectively, for each regression.14
RESULTS Patient Characteristics A total of 1746 patients were included in our study. Overall, these included 345 (19.8%) underweight, 952 (54.5%) normal weight, 209 (12.0%) overweight, and 240 (13.7%) obese children and adolescents. Specific weight class proportions based on the procedural group are indicated in Table 1 along with those preoperative variables showing significant rate discrepancies among the 4 weight groups, described below. Copyright
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J Pediatr Orthop
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BMI in Cerebral Palsy
Univariate Comparison of Demographics, Comorbidities, and Complications Table 1 contains a detailed list of those preoperative variables that significantly differed among weight classes for each procedural cohort. No other significant differences in preoperative variables existed among weight classes in any of the 3 procedural groups, including CPT codes (P = 0.061 to 0.374). In addition, 32.7% (osteotomies), 47.9% (spine), and 13.9% (tendon procedures) of underweight patients were receiving preoperative nutritional support with no significant differences in nutritional support among weight classes. Underweight CP patients had higher rates of sepsis (P = 0.003) in the osteotomy group and higher rates of bleeding in the spine surgery group (P = 0.025). In the spine cohort, obese patients had higher rates of wound disruption (P = 0.045) with no differences in complication rates in our univariate analysis in the tendon procedure group.
Multivariate Analyses With respect to osteotomy procedures, underweight class was an independent risk factor for developing any postoperative complication [odds ratio (OR) 1.72, 95% confidence interval (CI): 1.03-2.86, P = 0.037] and medical complication (OR 1.80, CI: 1.06-3.06, P = 0.031), whereas overweight class and obesity were not associated with any independent increased risk of any complication, any medical complication, or wound complications (Table 2). Similarly, underweight was associated with an increased risk of total complications (OR 1.99, CI: 1.11-3.59, P = 0.022) and medical complications (OR 1.95, CI: 1.12-3.41, P = 0.019) in the spine surgery cohort (Table 3). Finally, weight class was not independently associated with total complications or surgical site complications in CP patients receiving tendon procedures (Table 4). Multivariate analyses were not conducted on medical complications in the tendon surgery group or reoperations in the tendon surgery and osteotomy
group due to low 30-day incidences in those cohorts. Our c indices of 0.703-0.934 represented excellent predictive models.
DISCUSSION BMI in the pediatric population is an age-adjusted anthropometric measure used to appropriately assess growth development, nutritional status, and comorbidity burden.15 Underweight and obesity are extreme weight percentiles, and have been corroborated as risk factors for postsurgical morbidity and mortality. Underweight is a measure of malnutrition, which has been associated with increased risk of infections, numerous medical complications, and death in surgical patients.16–18 The nutritional demands of children in appropriate wound healing and recovery after operative intervention are fundamental in preventing short-term complications. Concurrently, obesity in children has been linked to surgical site infections, thromboembolic events, and decubitus ulcers.19,20 Obesity can involve thick subcutaneous adipose layers, which can form dead space after closure, increasing the risk for site infection and wound disruption through necrosis of local fat.21 Obesity has also been linked to numerous other comorbidities, which lends itself to poor postoperative courses. Alarmingly, the national rate of obesity has precipitously grown in the last few decades, with an associated increased incidence in children with CP.9 In our study of children and adolescents with CP undergoing orthopaedic procedures, the prevalence of underweight and obesity were 19.8% and 13.7%, respectively, similar to rates shown in previous literature.9 Our results demonstrate that underweight CP patients are independently at risk for 30-day postoperative complications after orthopaedic surgery, particularly medical complications, for both spine procedures and osteotomies. BMI class in tendon procedures, likely due to the low overall complication rate, did not affect morbidity and mortality. Univariate analysis demonstrated the
TABLE 1. Statistically Significant Discrepancies in Patient Demographics and Comorbidities Based on Weight Classification Patient Characteristic
Underweight [n (%)]
Hip or lower extremity osteotomy procedure (n = 467) n 104 Diabetes 0 (0.00) Asthma 12 (11.54) Chronic steroid use 1 (0.96) Spine procedure (n = 468) n 140 Diabetes 1 (0.71) Ventilator requirement 8 (5.71) Tracheostomy 4 (2.86) Tendon procedure (n = 811) n 101 Asthma 3 (2.97) CNS tumor 0 (0.00) Seizure disorder 32 (31.68) Chronic steroid use 1 (0.99) ASAZ3 53 (52.48)
P
Normal Weight [n (%)]
Overweight [n (%)]
Obese [n (%)]
247 0 (0.00) 27 (10.93) 1 (0.40)
51 0 (0.00) 13 (25.49) 1 (1.96)
65 2 (3.08) 15 (23.08) 5 (7.69)
0.006 0.007 0.021
241 1 (0.41) 14 (5.81) 17 (7.05)
44 0 (0.00) 8 (18.18) 7 (15.91)
43 2 (4.65) 3 (6.98) 4 (9.30)
0.041 0.026 0.022
39 0 87 0 132
464 (8.41) (0.00) (18.75) (0.00) (28.45)
9 0 21 0 34
114 (7.89) (0.00) (18.42) (0.00) (29.82)
14 2 31 3 38
132 (10.61) (1.52) (23.48) (2.27) (28.79)
0.021 0.016 0.026 0.008 < 0.001
ASA indicates American Society of Anesthesiologists; CNS, central nervous system.
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TABLE 2. Multivariate Analysis of Weight Classification on Complications in Hip or Lower Extremity Osteotomies (n = 467) 95% CI Weight Category Any complication Underweight Normal weight Overweight Obese Any surgical site complication Underweight Normal weight Overweight Obese Any medical complication Underweight Normal weight Overweight Obese
Odds Ratio
Lower
Upper
P
Hosmer-Lemeshow
c Statistic
1.72 REF 0.72 0.68
1.03 REF 0.33 0.32
2.86 REF 1.56 1.42
0.037* REF 0.397 0.302
0.316
0.730
1.77 REF 3.87 1.89
0.30 REF 0.50 0.14
10.36 REF 12.24 16.00
0.528 REF 0.196 0.635
0.907
0.926
1.80 REF 0.64 0.79
1.06 REF 0.28 0.36
3.06 REF 1.46 1.71
0.031* REF 0.290 0.310
0.153
0.763
*Significant value (Pr0.05). CI indicates confidence interval; REF, reference value.
highest rates of both postoperative bleeding requiring transfusion in spine surgery and sepsis in osteotomies in the underweight. Malnutrition is often associated with iron deficiency anemia, and hence may account for the postoperative transfusion requirement.22 Although it is possible that underweight patients underwent more extensive procedures, after stratification through procedures, no significant differences in CPT codes existed between weight classes. Malnutrition is also associated with impaired gut barrier function, low levels of complement, atrophied lymphatic tissue, reduced exocrine protective factors, and other immunologic aberrations, which place these patients at increased risk for systemic
infections.23 In addition, it has been shown that patients with more involved CP and higher Gross Motor Function Classification System (GMFCS) scores, and hence more involved surgical intervention, are also at a higher risk for malnutrition.8 Whereas low BMI was an independent risk factor for postoperative morbidity in CP patients, to our surprise, obesity was not, although higher rates of wound dehiscence were seen in obese patients after spine procedures. In pediatric orthopaedic surgery, although the impact of obesity on complications has been limited, the majority of studies demonstrate a strong association mostly with respect to long-term complication, not assessed with our data.24–28 It
TABLE 3. Multivariate Analysis of Weight Classification on Complications in Spine Procedures (n = 468) 95% CI Weight Category Any complication Underweight Normal weight Overweight Obese Any surgical site complication Underweight Normal weight Overweight Obese Any medical complication Underweight Normal Weight Overweight Obese Any unplanned reoperation Underweight Normal weight Overweight Obese
Odds Ratio
Lower
Upper
P
Hosmer-Lemeshow
c Statistic
1.99 REF 0.67 0.88
1.11 REF 0.31 0.4
3.59 REF 1.45 1.98
0.022* REF 0.31 0.762
0.240
0.739
0.50 REF 0.74 0.55
0.20 REF 0.16 0.12
1.28 REF 3.49 2.59
0.148 REF 0.704 0.453
0.354
0.763
1.95 REF 0.56 0.85
1.12 REF 0.26 0.38
3.41 REF 1.22 1.89
0.019* REF 0.145 0.689
0.126
0.703
0.53 REF 0.17 1.38
0.24 REF 0.02 0.51
1.17 REF 1.31 3.76
0.117 REF 0.088 0.530
0.384
0.726
*Significant value (Pr0.05). CI indicates confidence interval; REF, reference value.
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J Pediatr Orthop
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BMI in Cerebral Palsy
TABLE 4. Multivariate Analysis of Weight Classification on Complications in Tendon Procedures (n = 811) 95% CI Weight Category Any complication Underweight Normal weight Overweight Obese Any surgical site complication Underweight Normal weight Overweight Obese
Odds Ratio
Lower
Upper
P
Hosmer-Lemeshow
c Statistic
1.60 REF 0.44 0.20
0.32 REF 0.05 0.01
7.93 REF 4.33 3.77
0.563 REF 0.485 0.283
0.632
0.934
0.55 REF 0.76 1.08
0.06 REF 0.08 0.12
5.41 REF 6.99 10.19
0.610 REF 0.806 0.946
0.932
0.830
CI indicates confidence interval; REF, reference value.
is unclear why obese and overweight patients in our cohort do not have an increased risk of postoperative morbidity. One hypothesis is that obese patients may have less involved CP and increased functional status, which may play a potential protective role to offset the risk of adverse events typically associated with increasing body mass. Another conjecture is that the unaffected nutritional status in obese patients when compared with normal-weight patients supersedes the deleterious effects of elevated BMI. This implication endorses the importance of preoperative nutritional status with respect to risk stratification—namely that underweight CP children have an increased risk for complications, and hence require more extensive preoperative evaluation, risk counseling for parents, and postoperative care and monitoring. Fortunately, preoperative malnutrition is often subject to modification and improvement. Interestingly, although underweight patients had higher complications in spinal surgery and osteotomies, less than half of those patients were receiving preoperative nutritional support, and rates of nutritional support did not significantly vary among weight classes for any of our 3 procedure groups. Several studies have examined the role of postoperative nutritional supplementation, which have been shown to decrease rates of infection and hospital length of stay following orthopaedic procedures.29 Hence, more aggressive attempts to address nutritional status with specific preoperative nutrition plans in the underweight group before osteotomies and spinal intervention may improve outcomes. This study is not without limitations. First is the fact that the ACS-NSQIP pediatric database does not include information regarding the severity of CP or markers of functional status, such as the Gross Motor Function Classification System (GMFCS) score, and, although it includes nutritional support as a variable, it does not indicate poor nutritional status as many patients with this comorbidity may not be on supplementation. Functional and ambulatory status may be a confounder in our analysis of BMI and complication rates, and may be potentially responsible for the surprising result that obesity does not contribute to an increased risk for perioperative adverse events. This database also does not include geographic information, pediatric orthopaedic surgeon experience, and academic versus private Copyright
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hospital type—all of which may also be potential confounders. Furthermore, although the list of preoperative confounding comorbidities in our study is fairly extensive, there may be others not included in NSQIP that we were not able to control for. In addition, the 30-day window is an intrinsic limitation in our study, as complications can occur outside of this time interval. It is possible that certain weight classes such as obesity may have more long-term complications that cannot be evaluated with our data set. Specifically, our analysis does not shed light on a number of long-term complications, such as malunion, failure of hardware, cast complications, pain, and poor functional improvement, all of which have been associated in the obese pediatric population. Hence, readers must be mindful that our data do not demonstrate overall postoperative differences, but provides a commentary regarding disparities in short-term perioperative events between weight classes. Our results reveal certain complications that practitioners should be mindful of in the immediate postoperative period, which has implications for 30-day follow-up, surveillance, and management.
CONCLUSIONS We present a comprehensive evaluation of the effect of BMI on 30-day complications after pediatric orthopaedic surgery on patients with CP. To our knowledge, this is the largest and first national, multicentered analysis of weight classification and postoperative morbidity and mortality in the pediatric CP population. Underweight status was deemed an independent predictor of increased 30-day complications in certain procedures. This information can greatly aid providers with risk stratification, preoperative counseling, and postoperative monitoring as it relates to orthopaedic surgery. REFERENCES 1. Bax M, Goldstein M, Rosenbaum P, et al. Proposed definition and classification of cerebral palsy, April 2005. Dev Med Child Neurol. 2005;47:571–576. 2. Colver A, Fairhurst C, Pharoah PO. Cerebral palsy. Lancet. 2014;383:1240–1249. 3. Sponseller PD, Shah SA, Abel MF, et al. Infection rate after spine surgery in cerebral palsy is high and impairs results: multicenter analysis of risk factors and treatment. Clin Orthop Relat Res. 2010;468:711–716.
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4. Firth GB, Passmore E, Sangeux M, et al. Multilevel surgery for equinus gait in children with spastic diplegic cerebral palsy: mediumterm follow-up with gait analysis. J Bone Joint Surg Am. 2013;95: 931–938. 5. Mohamed Ali MH, Koutharawu DN, Miller F, et al. Operative and clinical markers of deep wound infection after spine fusion in children with cerebral palsy. J Pediatr Orthop. 2010;30:851–857. 6. Kuperminc MN, Stevenson RD. Growth and nutrition disorders in children with cerebral palsy. Dev Disabil Res Rev. 2008;14:137–146. 7. Chandra RK, Kumari S. Nutrition and immunity: an overview. J Nutr. 1994;124:1433s–1435s. 8. Feeley BT, Gollapudi K, Otsuka NY. Body mass index in ambulatory cerebral palsy patients. J Pediatr Orthop B. 2007; 16:165–169. 9. Rogozinski BM, Davids JR, Davis RB, et al. Prevalence of obesity in ambulatory children with cerebral palsy. J Bone Joint Surg Am. 2007;89:2421–2426. 10. Tahiri Y, Fischer JP, Wink JD, et al. Analysis of risk factors associated with 30-day readmissions following pediatric plastic surgery - a review of 5,376 procedures. Plast Reconstr Surg. 2014;2: 521–529. 11. Shah RK, Stey AM, Jatana KR, et al. Identification of opportunities for quality improvement and outcome measurement in pediatric otolaryngology. JAMA Otolaryngol Head Neck Surg. 2014;11:1019–1026. 12. Birkmeyer JD, Shahian DM, Dimick JB, et al. Blueprint for a new American College of Surgeons: National Surgical Quality Improvement Program. J Am Coll Surg. 2008;207:777–782. 13. Peduzzi P, Concato J, Kemper E, et al. A simulation study of the number of events per variable in logistic regression analysis. J Clin Epidemiol. 1996;49:1373–1379. 14. Merkow RP, Bilimoria KY, Hall BL. Interpretation of the Cstatistic in the context of ACS-NSQIP models. Ann Surg Oncol. 2011;18(suppl 3):S295–S296. 15. Lacher M, Froehlich S, von Schweinitz D, et al. Early and long term outcome in children with esophageal atresia treated over the last 22 years. Klin Padiatr. 2010;222:296–301. 16. Fu MC, Buerba RA, Grauer JN. Preoperative nutritional status as an adjunct predictor of major postoperative complications following
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anterior cervical discectomy and fusion. J Spinal Disord Tech. 2014. [Epub ahead of print]. O’Daly BJ, Walsh JC, Quinlan JF, et al. Serum albumin and total lymphocyte count as predictors of outcome in hip fractures. Clin Nutr. 2010;29:89–93. Koval KJ, Maurer SG, Su ET, et al. The effects of nutritional status on outcome after hip fracture. J Orthop Trauma. 1999;13:164–169. Rana AR, Michalsky MP, Teich S, et al. Childhood obesity: a risk factor for injuries observed at a level-1 trauma center. J Pediatr Surg. 2009;44:1601–1605. Brown CV, Neville AL, Salim A, et al. The impact of obesity on severely injured children and adolescents. J Pediatr Surg. 2006;41: 88–91; discussion 88-91. Mehta AI, Babu R, Karikari IO, et al. 2012 Young Investigator Award winner: the distribution of body mass as a significant risk factor for lumbar spinal fusion postoperative infections. Spine. 2012;37:1652–1656. Domellof M, Braegger C, Campoy C, et al. Iron requirements of infants and toddlers. J Pediatr Gastroenterol Nutr. 2014;58:119–129. Rytter MJ, Kolte L, Briend A, et al. The immune system in children with malnutrition—a systematic review. PloS one. 2014;9:e105017. Fedorak GT, Cuomo AV, Otsuka NY. Does pediatric body mass index affect surgical outcomes of lower-extremity external fixation? J Pediatr Orthop. 2014. [Epub ahead of print]. Burghardt RD, Specht SC, Herzenberg JE. Mechanical failures of eight-plateguided growth system for temporary hemiepiphysiodesis. J Pediatr Orthop. 2010;30:594–597. Linam WM, Margolis PA, Staat MA, et al. Risk factors associated with surgical site infection after pediatric posterior spinal fusion procedure. Infect Control Hosp Epidemiol. 2009;30:109–116. Leet AI, Pichard CP, Ain MC. Surgical treatment of femoral fractures in obese children: does excessive body weight increase the rate of complications? J Bone Joint Surg Am. 2005;87:2609–2613. Weiss JM, Choi P, Ghatan C, et al. Complications with flexible nailing of femur fractures more than double with child obesity and weight > 50 kg. J Child Orthop. 2009;3:53–58. Lawson RM, Doshi MK, Barton JR, et al. The effect of unselected post-operative nutritional supplementation on nutritional status and clinical outcome of orthopaedic patients. Clin Nutr. 2003;22:39–46.
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