Review Article
Evaluation of Malnutrition in Orthopaedic Surgery Abstract Michael Brian Cross, MD Paul Hyunsoo Yi Charlotte F. Thomas Jane Garcia, RN Craig J. Della Valle, MD
From the Department of Orthopaedic Surgery, Rush University Medical Center, Chicago, IL. Dr. Della Valle or an immediate family member serves as a paid consultant to Biomet, ConvaTec, DePuy, and Smith & Nephew; has stock or stock options held in CD Diagnostics; has received research or institutional support from Biomet, CD Diagnostics, Smith & Nephew, and Stryker; and serves as a board member, owner, officer, or committee member of the American Association of Hip and Knee Surgeons, the Arthritis Foundation, and The Knee Society. None of the following authors or any immediate family member has received anything of value from or has stock or stock options held in a commercial company or institution related directly or indirectly to the subject of this article: Dr. Cross, Mr. Yi, Ms. Thomas, and Ms. Garcia. J Am Acad Orthop Surg 2014;22: 193-199 http://dx.doi.org/10.5435/ JAAOS-22-03-193 Copyright 2014 by the American Academy of Orthopaedic Surgeons.
March 2014, Vol 22, No 3
Malnutrition can increase the risk of surgical site infection in both elective spine surgery and total joint arthroplasty. Obesity and diabetes are common comorbid conditions in patients who are malnourished. Despite the relatively high incidence of nutritional disorders among patients undergoing elective orthopaedic surgery, the evaluation and management of malnutrition is not generally well understood by practicing orthopaedic surgeons. Serologic parameters such as total lymphocyte count, albumin level, prealbumin level, and transferrin level have all been used as markers for nutrition status. In addition, anthropometric measurements, such as calf and arm muscle circumference or triceps skinfold, and standardized scoring systems, such as the Rainey-MacDonald nutritional index, the Mini Nutritional Assessment, and institution-specific nutritional scoring tools, are useful to define malnutrition. Preoperative nutrition assessment and optimization of nutritional parameters, including tight glucose control, normalization of serum albumin, and safe weight loss, may reduce the risk of perioperative complications, including infection.
T
he term “malnutrition” has been used interchangeably with “nutrient deficiency” in some of the orthopaedic literature.1,2 However, according to the World Health Organization, malnutrition encompasses both deficiencies and excesses in nutrients.3 In fact, nutrient deficiencies (ie, caloric overnourishment) are highly prevalent in persons with obesity, which may be a contributing factor to the development of diabetes mellitus (DM) in this patient population.4 DM is an extensive topic, and glucose intolerance and DM are discussed in depth elsewhere. For the purposes of this article, we define malnutrition generally as any disorder of nutrition, including deficiency of nutrients or excess of nutrients (ie, obesity). Malnutrition has been shown to be associated
with increased morbidity in orthopaedic surgery.
Definition of Malnutrition In the orthopaedic literature, malnutrition has been defined using a variety of methods, including serologic laboratory values,1,5-7 anthropometric measurements,6,8-10 and standardized nutrition scoring tools11-13 (Table 1). In relation to surgical site infection (SSI) or impaired wound healing— a risk factor for SSI14—the most common definitions of malnutrition are a serum total lymphocyte count ,1,500 cells per cubic millimeter and a serum albumin concentration of ,3.5 g/dL.1,5,12,14 The total lymphocyte count is calculated by multiplying the serum white blood cell count by the percentage of lymphocytes in the differential. Low serum
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Evaluation of Malnutrition in Orthopaedic Surgery
Table 1 Methods of Evaluating Malnutrition Method Serologic laboratory values Anthropometric measurements
Standardized scoring tools
Advantages
Sensitive indicators of even marginal or acute Total lymphocyte count ,1,500 cells/mm3, nutritional deficiency.5,10 Most commonly serum albumin level ,3.5 g/dL, serum transferrin ,200 mg/dL used method(s) in the literature.1,14 Indirect indicators of undernutrition via body Calf muscle circumference ,31 cm,15 arm composition measurement.5 Cheaply and muscle circumference ,22 mm,15 triceps easily performed. Cannot detect marginal or skinfold (no definitive cutoff, but lower values acute undernutrition,5 but they better reflect indicate worse nutrition)8 long-term changes in nutritional status than do serologic laboratory values.8 Rainey-MacDonald nutritional index,6,11,12 Mini Standardized and easy-to-interpret measurement of nutritional status. Potentially Nutritional Assessment,6,15 Schwarzkopf robust assessment via consideration of nutritional index (NYU Hospital for Joint different variables. To ensure validity and Diseases–specific)13 reliability, each tool must be formally tested, even if adapted from validated surveys.
prealbumin6,7,13,16 and serum transferrin levels ,200 mg/dL1,14,17 are also considered signs of malnutrition. Although it is not a universally established assessment of nutrition, a low preoperative zinc level (ie, ,95 mg/dL) has also been associated with impaired wound healing following orthopaedic surgery.14 Albumin, prealbumin, and transferrin are visceral proteins that are sensitive indicators of marginal nutrient deficiency, and they can be used to detect acute nutritional changes by virtue of their short half-lives.5,10 Prealbumin, however, has not been used as extensively to assess perioperative nutrition, perhaps because this parameter is too sensitive to accurately reflect changes in protein-caloric nutrition.6 No established definition of malnutrition using prealbumin exists in the orthopaedic literature. The normal range of prealbumin is approximately 16 to 35 mg/dL.18 Similarly, controversy exists regarding the validity of the total lymphocyte count as a marker of nutrition.19 Even so, it is still used frequently in the literature to define malnutrition.1,5,6,17 Albumin level is one of the most widely recognized and simplest markers of nutritional status.
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Parameters
Undernutrition has also been defined in the orthopaedic literature by way of anthropometric measurements, such as calf circumference,6,15 arm muscle circumference,6,9,10,15 and triceps skinfold.8 Specifically, undernutrition in adults has been defined as calf circumference ,31 cm or an arm muscle circumference ,22 cm.15 Arm muscle circumference of 60% to 90% of the standard for a particular sex is a marker of moderate malnutrition, and circumference ,60% is a marker of severe malnutrition.9 Although the triceps skinfold test is a poorly described tool for assessing nutrition, it continues to be used in the orthopaedic literature.8 Anthropometric measurements serve as an indirect gauge of undernutrition by providing insight into body composition.5 Body fat and skeletal muscle are depleted late in the course of malnourishment; thus, anthropometric tools cannot be used detect marginal malnutrition or acute changes in nutrition status.5 However, these tools are good indicators of chronic changes in nutritional status.8 Furthermore, anthropometric measurements are inexpensive and easily performed, and they can yield valuable information regarding a patient’s nutrition status.
Standardized malnutrition screening tools and malnutrition assessment tools are also used to define malnutrition. The Rainey-MacDonald nutritional index (RMNI) has been used in several studies.6,11,12 It is calculated from serum albumin and serum transferrin:
RMNI5ð1:2·serum albuminÞ1ð0:013·serum transferrinÞ26:43:6;20 A zero or negative score indicates nutritional depletion. The RMNI has not been validated.6 The multi-question Mini Nutritional Assessment (MNA) has been shown to be reliable in assessing malnutrition in the geriatric population6,15,21 (Figure 1). The MNA includes questions on a variety of topics, such as anthropometric measures and dietary habits, which allows for a sophisticated measurement of malnourishment that takes into account multiple variables that affect nutritional status. A difference exists between screening nutritional tools and assessment tools. However, Ozkalkanli et al13 demonstrated that the odds ratio of the association between malnutrition
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Figure 1
The Mini Nutritional Assessment form. (Copyright Nestlé, 1994, Revision 2009.)
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(ie, assessment tools) or the risk of malnutrition (ie, screening tools) and morbidity in orthopaedic surgery is 3.5 and 4.1, respectively. Thus, both types of tool can be used to predict increased morbidity following orthopaedic surgery. The World Health Organization classified obesity thus: class I, body mass index (BMI) 30.0 to 34.9 kg/m2; class II, BMI 35 to 39.9 kg/m2; and class III, BMI $40 kg/m2.22 The diagnostic criteria for DM are listed in Table 2.
Mechanisms for Malnutrition in Increasing Infection Risk Malnutrition is thought to predispose patients to SSI1,24-26 by impairing wound healing6,11,17 and prolonging inflammation via several mechanisms, including impaired fibroblast proliferation and collagen synthesis.27 Decreased lymphocyte count is thought to impair the ability of the immune system to eradicate or prevent infection. Obesity contributes to SSI by making it difficult to achieve adequate wound closure and through the process of fat necrosis, leading to impaired healing and the creation of dead space, which can lead to problems with local wound healing.27 Obesity is associated with increased surgical time, which further increases the risk of infection.28 DM predisposes patients to SSI by preventing the adequate utilization of glucose for energy and adequate oxygen delivery secondary to glycosylation of hemoglobin and micro- and macrovascular disease, which ultimately results in ischemic tissue that is more susceptible to infection.27
Malnutrition and SSI in Spine Surgery Both superficial and deep SSI after orthopaedic spinal surgery have been linked to several markers of malnu-
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trition, including serologic laboratory values, DM, hyperglycemia, and obesity.29-34 Because the risk of deep infection has been shown to be higher in patients with neuromuscular conditions, most research in spine surgery has been done to identify risk factors, including malnutrition, that may increase the risk of infection in this patient population. Whether poor preoperative nutrition as defined by serologic laboratory measurements increases the risk of deep infection after spinal surgery is a point of contention in the literature, however. Jevsevar and Karlin30 reported that preoperative albumin $3.5 mg/dL and total lymphocyte count $1,500 cells per cubic millimeter were associated with lower rates of overall infection in 44 patients with cerebral palsy after spinal surgery. Similarly, in a review of patients undergoing elective spine surgery, Beiner et al7 reported higher rates of postoperative infection and poor wound healing in patients with serum albumin levels ,3.5 mg/dL and total lymphocyte counts ,1,500 per cubic millimeter. Although most of the literature demonstrates an association between these serologic laboratory values and infection, a retrospective multicenter case-control study of 210 neuromuscular scoliosis surgeries found no statistically significant association between undernutrition, as defined by serum albumin ,3.5 mg/dL and total lymphocyte count ,1,500 per cubic millimeter, and increased risk of infection.31 In 2007, Friedman et al32 compared 41 cases of SSIs after laminectomy with 82 matched control subjects at a single site. Both DM and BMI .35 kg/m2 were found to be independent risk factors for SSI, with odds ratios of 4.2 and 7.1, respectively. In a case-control study published in 2008, 46 patients with SSI after spine surgery were compared with 227 uninfected control patients.33 Obesity
(ie, BMI of 30 to 35 kg/m2), DM, an elevated preoperative serum glucose level (.125 mg/dL), and postoperative serum glucose levels .200 mg/dL all were associated with increased risk of SSI. Thus, the risk of infection was higher even in patients who did not have a diagnosis of DM, which suggests that hyperglycemia and blood glucose impairment alone increase the risk of SSI, regardless whether the patient has a diagnosis of DM.4 A subsequent retrospective cohort analysis of 3,174 spinal surgeries at a single center corroborated these results by showing that DM was an independent risk factor for SSI and that obesity (BMI .30 kg/m2) increased the risk of superficial infection.34
Malnutrition and Total Joint Arthroplasty Malnutrition in several forms has been associated with increased risk of infection and impaired wound healing following total joint arthroplasty. Peersman et al24 retrospectively reviewed 6,489 total knee arthroplasties (TKAs) at a single site over 7 years and reported 97 prosthetic joint infections (PJIs). Compared with matched control patients, the factors of poor nutrition, obesity, and DM were found to increase the risk of PJI. Malnutrition has also been associated with persistent wound drainage and PJI.5 The impact of nutritional status on wound drainage and subsequent deep PJI was investigated in a retrospective review of 11,785 consecutive lower extremity arthroplasty procedures.1 Eighty-three patients had persistent wound drainage following irrigation and débridement and had further surgery. Of the patients who failed the additional surgical treatment and went on to develop deep infection, 35% were found to be undernourished (ie, serum albumin ,3.5 g/dL, total lymphocyte count ,1,500 per cubic millimeter, or transferrin
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Table 2 The Four Diagnostic Criteria for Diabetes Mellitus According to the American Diabetes Association23 Hemoglobin A1c $6.5% Fasting ($8 h) plasma glucose levels $126 mg/dL (or 7 mmol/L) Two-hour plasma glucose $200 mg/dL (11.1 mmol/L) during an oral glucose tolerance test Classic symptoms of hyperglycemia (eg, polydipsia, polyuria) or hyperglycemic crisis and random plasma glucose $200 mg/dL (11.1 mmol/L)
,200 mg/dL). The success rate of the initial irrigation and débridement in the malnourished population was only 5%. Font-Vizcarra et al8 prospectively studied 213 patients who underwent TKA and found malnutrition, as indicated by smaller triceps skinfold measurement, to be independently associated with both superficial and deep infection. Specifically, a triceps skinfold measurement of 30 mm was associated with a 5% risk of infection. The risk of infection was 10% with a skinfold measurement of 20 mm. The relationship between obesity and PJI has been studied extensively.24-26,28,35-37 In a prospective study of 1,509 consecutive TKAs, Chesney et al35 found that although morbid obesity (BMI .40 kg/m2) increased the odds for deep infection, it did not reach statistical significance. However, in a retrospective study, Peersman et al24 found that obesity significantly increased the risk of PJI. Similarly, in a retrospective review of 6,108 total hip arthroplasties (THAs) and TKAs, Malinzak et al28 found the odds for PJI to be 21.3 times greater in patients with BMI .50 kg/m2. The authors of a prospective study of 1,214 consecutive primary TKAs found that patients with morbid obesity (BMI $40 kg/m2) had a nine times greater risk of having a PJI after surgery compared with patients who were not obese.36 Diabetes combined with obesity further increased that risk. Patients with BMI of 30 to 39 kg/m2 were not at increased risk of infection. March 2014, Vol 22, No 3
In 2012, Bozic and colleagues published two separate analyses of the Medicare 5% claims database— one on TKA25 and the other on THA.26 The patient sample size was 83,011 in the TKA study and 40,919 in the THA study. In both studies, the diagnosis of obesity, which was filed in either inpatient or outpatient Medicare claims submitted during the 12 months before the operation, was found to be a statistically significant risk factor for PJI. Not all studies are definitive, however. In 2011, Davis et al37 published the results of a prospective study of 1,617 consecutive primary THAs performed in England. Although increased BMI (.35 kg/m2) was significantly associated with superficial infections, with an 89.5% increase in superficial infections per 10-point rise in BMI, it did not reach statistical significance for association with deep infection. However, this may have been due to the small number of deep infections in this series (15 total). Patients with obesity should be encouraged to lose weight and undergo a nutritional consultation before surgery. For patients with BMI .40 kg/m2, it is particularly important to assess baseline nutritional status and construct a meal plan designed for safe weight loss. Coexisting nutritional impairments should be corrected as well, including vitamin D deficiency, which is present in 80% to 90% of patients with obesity.4 Ensuring gradual, safe weight loss is important because rapid weight loss may cause undernourishment in some patients,34 which would simply replace one
nutritional disorder for another. Bariatric surgery may be an option before elective procedures because it may lessen the operative time, the anesthesia time, and the risk of perioperative complications; however, little has been published on this topic.38,39 The relationship between blood glucose impairment and DM and deep infections has been well-studied in the orthopaedic literature.25,26,28,35,36,40,41 Several studies have shown DM to be a risk factor for deep infection.25,26,28,35 Similarly, in a retrospective study, Jämsen et al40 reported that preoperative hyperglycemia (blood glucose level $110 mg/dL) was associated with higher risk of PJI. In 2009, Dowsey and Choong36 demonstrated that PJI occurred in patients with DM only if they had obesity. Thus, the authors postulated that there may be interaction between the two diseases, possibly involving the impact of obesity on blood glucose (ie, hyperglycemia). Although some studies demonstrate an increased risk of infection in patients with hemoglobin A1c .6.5%,42 a retrospective cohort study of 350 persons with diabetes and with varying degrees of DM control as measured by hemoglobin A1c level (,7% or $7%) found no statistically significant difference in incidence of SSI between the two groups.41
Summary and Clinical Recommendations Given the prevalence of malnutrition in orthopaedic patients and the impact
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on the outcomes and complications of orthopaedic procedures, the surgeon should assess preoperative serum albumin level, total lymphocyte count, and transferrin level, and patients whose laboratory values fall below the cutoffs described above should undergo a nutritional consultation. Patients with DM should work to achieve improved glucose control, and they should be carefully monitored postoperatively. In our practice, we routinely obtain a hemoglobin A1c value preoperatively and discuss with the patient delaying elective surgery if that value exceeds 7%. Similarly, patients with obesity can attempt healthy weight loss with the help of a multidisciplinary team that includes a dietician, physical therapist, and internal medicine specialist. Unfortunately, medical insurance programs such as Medicaid do not cover such services. Although anthropometric measurements have been shown to be useful indicators of malnutrition in patients undergoing orthopaedic surgery,6,9,10 we do not recommend their use at this time because standardized cutoff values have not been established and because their use is not as well substantiated as use of serologic laboratory values. We do not recommend obtaining serum prealbumin levels because they are too sensitive to accurately reflect changes in protein-calorie nutrition.6 Standardized nutritional scoring systems that may be used as a substitute for serologic parameters include the RMNI,6,10,11 MNA,6,15 Nutritional Risk Screening 2002,13 and the subjective global assessment.13 If a patient is found to be malnourished, we recommend discussing with the patient the possibility of delaying elective surgery until the patient’s nutritional status has improved. To our knowledge, no study has shown improved outcomes as a result of correcting nutritional status preoperatively; however, given that the literature supports a link between
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malnutrition and increased morbidity after orthopaedic surgery, we believe that addressing malnutrition preoperatively is a reasonable approach in the attempt to reduce the risk of complications. Future studies should focus on whether improving preoperative nutritional status improves patient outcomes by decreasing the risk of morbidity after orthopaedic surgery.
nutritional status and post-operative infection in total knee replacements: A prospective study of 213 patients. Int J Artif Organs 2011;34(9):876-881. 9. Pratt WB, Veitch JM, McRoberts RL: Nutritional status of orthopedic patients with surgical complications. Clin Orthop Relat Res 1981;(155):81-84. 10. Jensen JE, Jensen TG, Smith TK, Johnston DA, Dudrick SJ: Nutrition in orthopaedic surgery. J Bone Joint Surg Am 1982;64(9):1263-1272. 11. Rai J, Gill SS, Kumar BR: The influence of preoperative nutritional status in wound healing after replacement arthroplasty. Orthopedics 2002;25(4):417-421.
References Evidence-based Medicine: Levels of evidence are described in the table of contents. In this article, references 8, 12-14, 17, 19, 24-26, 35-37, 40, and 41 are level II studies. References 1, 5, 6, 9, 10, 16, 28, 30-34, 39, and 42 are level III studies. References 11, 15, and 29 are level IV studies. Reference 27 is level V expert opinion. References printed in bold type are those published within the past 5 years. 1. Jaberi FM, Parvizi J, Haytmanek CT, Joshi A, Purtill J: Procrastination of wound drainage and malnutrition affect the outcome of joint arthroplasty. Clin Orthop Relat Res 2008;466(6):1368-1371. 2. Smith TK: Nutrition: Its relationship to orthopedic infections. Orthop Clin North Am 1991;22(3):373-377. 3. World Health Organization: WHO, Nutrition Experts Take Action on Malnutrition. Available at: http://www.who.int/nutrition/ pressnote_action_on_malnutrition/en/. Accessed December 17, 2013. 4. Via M: The malnutrition of obesity: Micronutrient deficiencies that promote diabetes. ISRN Endocrinol 2012;2012: 103472. 5. Greene KA, Wilde AH, Stulberg BN: Preoperative nutritional status of total joint patients: Relationship to postoperative wound complications. J Arthroplasty 1991; 6(4):321-325. 6. Guo JJ, Yang H, Qian H, Huang L, Guo Z, Tang T: The effects of different nutritional measurements on delayed wound healing after hip fracture in the elderly. J Surg Res 2010;159(1):503-508. 7. Beiner JM, Grauer J, Kwon BK, Vaccaro AR: Postoperative wound infections of the spine. Neurosurg Focus 2003;15(3):E14. 8. Font-Vizcarra L, Lozano L, Ríos J, Forga MT, Soriano A: Preoperative
12. Puskarich CL, Nelson CL, Nusbickel FR, Stroope HF: The use of two nutritional indicators in identifying long bone fracture patients who do and do not develop infections. J Orthop Res 1990;8(6): 799-803. 13. Ozkalkanli MY, Ozkalkanli DT, Katircioglu K, Savaci S: Comparison of tools for nutrition assessment and screening for predicting the development of complications in orthopedic surgery. Nutr Clin Pract 2009;24(2):274-280. 14. Zorrilla P, Gómez LA, Salido JA, Silva A, López-Alonso A: Low serum zinc level as a predictive factor of delayed wound healing in total hip replacement. Wound Repair Regen 2006;14(2):119-122. 15. Murphy MC, Brooks CN, New SA, Lumbers ML: The use of the MiniNutritional Assessment (MNA) tool in elderly orthopaedic patients. Eur J Clin Nutr 2000;54(7):555-562. 16. McPhee IB, Williams RP, Swanson CE: Factors influencing wound healing after surgery for metastatic disease of the spine. Spine (Phila Pa 1976) 1998;23(6):726-732, discussion 732-733. 17. Gherini S, Vaughn BK, Lombardi AV Jr, Mallory TH: Delayed wound healing and nutritional deficiencies after total hip arthroplasty. Clin Orthop Relat Res 1993; (293):188-195. 18. Beck FK, Rosenthal TC: Prealbumin: A marker for nutritional evaluation. Am Fam Physician 2002;65(8):1575-1578. 19. Cereda E, Pusani C, Limonta D, Vanotti A: The association of Geriatric Nutritional Risk Index and total lymphocyte count with short-term nutrition-related complications in institutionalised elderly. J Am Coll Nutr 2008;27(3):406-413. 20. Rainey-Macdonald CG, Holliday RL, Wells GA, Donner AP: Validity of a twovariable nutritional index for use in selecting candidates for nutritional support. JPEN J Parenter Enteral Nutr 1983;7(1):15-20.
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Copyright Ó the American Academy of Orthopaedic Surgeons. Unauthorized reproduction of this article is prohibited.
Michael Brian Cross, MD, et al 21. Guigoz Y: The Mini Nutritional Assessment (MNA) review of the literature: What does it tell us? J Nutr Health Aging 2006;10(6):466-485, discussion 485-487.
29. Li Y, Glotzbecker M, Hedequist D: Surgical site infection after pediatric spinal deformity surgery. Curr Rev Musculoskelet Med 2012; Feb 9 [Epub ahead of print].
22. World Health Organization: BMI Classification. Available at: http://apps. who.int/bmi/index.jsp?introPage=intro_3. html. Accessed January 13, 2014.
30. Jevsevar DS, Karlin LI: The relationship between preoperative nutritional status and complications after an operation for scoliosis in patients who have cerebral palsy. J Bone Joint Surg Am 1993;75(6):880-884.
23. American Diabetes Association: Diagnosis and classification of diabetes mellitus. Diabetes Care 2011;34(suppl 1):S62-S69. 24. Peersman G, Laskin R, Davis J, Peterson M: Infection in total knee replacement: A retrospective review of 6489 total knee replacements. Clin Orthop Relat Res 2001; (392):15-23. 25. Bozic KJ, Lau E, Kurtz S, Ong K, Berry DJ: Patient-related risk factors for postoperative mortality and periprosthetic joint infection in Medicare patients undergoing TKA. Clin Orthop Relat Res 2012;470(1):130-137. 26. Bozic KJ, Lau E, Kurtz S, et al: Patientrelated risk factors for periprosthetic joint infection and postoperative mortality following total hip arthroplasty in Medicare patients. J Bone Joint Surg Am 2012;94(9):794-800. 27. Seibert DJ: Pathophysiology of surgical site infection in total hip arthroplasty. Am J Infect Control 1999;27(6):536-542. 28. Malinzak RA, Ritter MA, Berend ME, Meding JB, Olberding EM, Davis KE: Morbidly obese, diabetic, younger, and unilateral joint arthroplasty patients have elevated total joint arthroplasty infection rates. J Arthroplasty 2009;24(6 suppl): 84-88.
31. Sponseller PD, LaPorte DM, Hungerford MW, Eck K, Bridwell KH, Lenke LG: Deep wound infections after neuromuscular scoliosis surgery: A multicenter study of risk factors and treatment outcomes. Spine (Phila Pa 1976) 2000;25(19):2461-2466. 32. Friedman ND, Sexton DJ, Connelly SM, Kaye KS: Risk factors for surgical site infection complicating laminectomy. Infect Control Hosp Epidemiol 2007;28(9): 1060-1065.
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Davis AM, Wood AM, Keenan AC, Brenkel IJ, Ballantyne JA: Does body mass index affect clinical outcome postoperatively and at five years after primary unilateral total hip replacement performed for osteoarthritis? A multivariate analysis of prospective data. J Bone Joint Surg Br 2011;93(9):1178-1182.
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Severson EP, Singh JA, Browne JA, Trousdale RT, Sarr MG, Lewallen DG: Total knee arthroplasty in morbidly obese patients treated with bariatric surgery: A comparative study. J Arthroplasty 2012;27 (9):1696-1700.
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Kulkarni A, Jameson SS, James P, Woodcock S, Muller S, Reed MR: Does bariatric surgery prior to lower limb joint replacement reduce complications? Surgeon 2011;9(1):18-21.
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Jämsen E, Nevalainen P, Eskelinen A, Huotari K, Kalliovalkama J, Moilanen T: Obesity, diabetes, and preoperative hyperglycemia as predictors of periprosthetic joint infection: A single-center analysis of 7181 primary hip and knee replacements for osteoarthritis. J Bone Joint Surg Am 2012;94(14):e101.
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Iorio R, Williams KM, Marcantonio AJ, Specht LM, Tilzey JF, Healy WL: Diabetes mellitus, hemoglobin A1C, and the incidence of total joint arthroplasty infection. J Arthroplasty 2012;27(5): 726-729, e1.
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Jämsen E, Nevalainen P, Kalliovalkama J, Moilanen T: Preoperative hyperglycemia predicts infected total knee replacement. Eur J Intern Med 2010;21(3):196-201.
33. Olsen MA, Nepple JJ, Riew KD, et al: Risk factors for surgical site infection following orthopaedic spinal operations. J Bone Joint Surg Am 2008;90(1):62-69. 34. Pull ter Gunne AF, Cohen DB: Incidence, prevalence, and analysis of risk factors for surgical site infection following adult spinal surgery. Spine (Phila Pa 1976) 2009;34 (13):1422-1428. 35. Chesney D, Sales J, Elton R, Brenkel IJ: Infection after knee arthroplasty: A prospective study of 1509 cases. J Arthroplasty 2008;23(3):355-359. 36. Dowsey MM, Choong PF: Obese diabetic patients are at substantial risk for deep infection after primary TKA. Clin Orthop Relat Res 2009;467(6):1577-1581.
Erratum Fresh Osteochondral Allograft Transplantation for the Knee: Current Concepts Seth L. Sherman, MD, Joseph Garrity, MS, Kathryn Bauer, James Cook, DVM, PhD, James Stannard, MD, and William Bugbee, MD (Vol 22, No 2, February 2014, pp 121-133) On the title page of this article, the MD degree was inadvertently deleted following Dr. Bauer’s name and, in the author notes, was incorrectly inserted after Mr. Garrity’s name. The byline should correctly read Seth L. Sherman, MD, Joseph Garrity, MS, Kathryn Bauer, MD, James Cook, DVM, PhD, James Stannard, MD, William Bugbee, MD. In the author notes near the bottom of the title page and in the disclosure paragraph at the bottom of the second article page, these authors’ names should read Mr. Garrity (rather than Dr. Garrity) and Dr. Bauer (rather than Ms. Bauer). The Journal regrets the error.
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Evaluation of Malnutrition in Orthopaedic Surgery Abstract Michael Brian Cross, MD Paul Hyunsoo Yi Charlotte F. Thomas Jane Garcia, RN Craig J. Della Valle, MD
From the Department of Orthopaedic Surgery, Rush University Medical Center, Chicago, IL. Dr. Della Valle or an immediate family member serves as a paid consultant to Biomet, ConvaTec, DePuy, and Smith & Nephew; has stock or stock options held in CD Diagnostics; has received research or institutional support from Biomet, CD Diagnostics, Smith & Nephew, and Stryker; and serves as a board member, owner, officer, or committee member of the American Association of Hip and Knee Surgeons, the Arthritis Foundation, and The Knee Society. None of the following authors or any immediate family member has received anything of value from or has stock or stock options held in a commercial company or institution related directly or indirectly to the subject of this article: Dr. Cross, Mr. Yi, Ms. Thomas, and Ms. Garcia. J Am Acad Orthop Surg 2014;22: 193-199 http://dx.doi.org/10.5435/ JAAOS-22-03-193 Copyright 2014 by the American Academy of Orthopaedic Surgeons.
March 2014, Vol 22, No 3
Malnutrition can increase the risk of surgical site infection in both elective spine surgery and total joint arthroplasty. Obesity and diabetes are common comorbid conditions in patients who are malnourished. Despite the relatively high incidence of nutritional disorders among patients undergoing elective orthopaedic surgery, the evaluation and management of malnutrition is not generally well understood by practicing orthopaedic surgeons. Serologic parameters such as total lymphocyte count, albumin level, prealbumin level, and transferrin level have all been used as markers for nutrition status. In addition, anthropometric measurements, such as calf and arm muscle circumference or triceps skinfold, and standardized scoring systems, such as the Rainey-MacDonald nutritional index, the Mini Nutritional Assessment, and institution-specific nutritional scoring tools, are useful to define malnutrition. Preoperative nutrition assessment and optimization of nutritional parameters, including tight glucose control, normalization of serum albumin, and safe weight loss, may reduce the risk of perioperative complications, including infection.
T
he term “malnutrition” has been used interchangeably with “nutrient deficiency” in some of the orthopaedic literature.1,2 However, according to the World Health Organization, malnutrition encompasses both deficiencies and excesses in nutrients.3 In fact, nutrient deficiencies (ie, caloric overnourishment) are highly prevalent in persons with obesity, which may be a contributing factor to the development of diabetes mellitus (DM) in this patient population.4 DM is an extensive topic, and glucose intolerance and DM are discussed in depth elsewhere. For the purposes of this article, we define malnutrition generally as any disorder of nutrition, including deficiency of nutrients or excess of nutrients (ie, obesity). Malnutrition has been shown to be associated
with increased morbidity in orthopaedic surgery.
Definition of Malnutrition In the orthopaedic literature, malnutrition has been defined using a variety of methods, including serologic laboratory values,1,5-7 anthropometric measurements,6,8-10 and standardized nutrition scoring tools11-13 (Table 1). In relation to surgical site infection (SSI) or impaired wound healing— a risk factor for SSI14—the most common definitions of malnutrition are a serum total lymphocyte count ,1,500 cells per cubic millimeter and a serum albumin concentration of ,3.5 g/dL.1,5,12,14 The total lymphocyte count is calculated by multiplying the serum white blood cell count by the percentage of lymphocytes in the differential. Low serum
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Evaluation of Malnutrition in Orthopaedic Surgery
Table 1 Methods of Evaluating Malnutrition Method Serologic laboratory values Anthropometric measurements
Standardized scoring tools
Advantages
Sensitive indicators of even marginal or acute Total lymphocyte count ,1,500 cells/mm3, nutritional deficiency.5,10 Most commonly serum albumin level ,3.5 g/dL, serum transferrin ,200 mg/dL used method(s) in the literature.1,14 Indirect indicators of undernutrition via body Calf muscle circumference ,31 cm,15 arm composition measurement.5 Cheaply and muscle circumference ,22 mm,15 triceps easily performed. Cannot detect marginal or skinfold (no definitive cutoff, but lower values acute undernutrition,5 but they better reflect indicate worse nutrition)8 long-term changes in nutritional status than do serologic laboratory values.8 Rainey-MacDonald nutritional index,6,11,12 Mini Standardized and easy-to-interpret measurement of nutritional status. Potentially Nutritional Assessment,6,15 Schwarzkopf robust assessment via consideration of nutritional index (NYU Hospital for Joint different variables. To ensure validity and Diseases–specific)13 reliability, each tool must be formally tested, even if adapted from validated surveys.
prealbumin6,7,13,16 and serum transferrin levels ,200 mg/dL1,14,17 are also considered signs of malnutrition. Although it is not a universally established assessment of nutrition, a low preoperative zinc level (ie, ,95 mg/dL) has also been associated with impaired wound healing following orthopaedic surgery.14 Albumin, prealbumin, and transferrin are visceral proteins that are sensitive indicators of marginal nutrient deficiency, and they can be used to detect acute nutritional changes by virtue of their short half-lives.5,10 Prealbumin, however, has not been used as extensively to assess perioperative nutrition, perhaps because this parameter is too sensitive to accurately reflect changes in protein-caloric nutrition.6 No established definition of malnutrition using prealbumin exists in the orthopaedic literature. The normal range of prealbumin is approximately 16 to 35 mg/dL.18 Similarly, controversy exists regarding the validity of the total lymphocyte count as a marker of nutrition.19 Even so, it is still used frequently in the literature to define malnutrition.1,5,6,17 Albumin level is one of the most widely recognized and simplest markers of nutritional status.
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Parameters
Undernutrition has also been defined in the orthopaedic literature by way of anthropometric measurements, such as calf circumference,6,15 arm muscle circumference,6,9,10,15 and triceps skinfold.8 Specifically, undernutrition in adults has been defined as calf circumference ,31 cm or an arm muscle circumference ,22 cm.15 Arm muscle circumference of 60% to 90% of the standard for a particular sex is a marker of moderate malnutrition, and circumference ,60% is a marker of severe malnutrition.9 Although the triceps skinfold test is a poorly described tool for assessing nutrition, it continues to be used in the orthopaedic literature.8 Anthropometric measurements serve as an indirect gauge of undernutrition by providing insight into body composition.5 Body fat and skeletal muscle are depleted late in the course of malnourishment; thus, anthropometric tools cannot be used detect marginal malnutrition or acute changes in nutrition status.5 However, these tools are good indicators of chronic changes in nutritional status.8 Furthermore, anthropometric measurements are inexpensive and easily performed, and they can yield valuable information regarding a patient’s nutrition status.
Standardized malnutrition screening tools and malnutrition assessment tools are also used to define malnutrition. The Rainey-MacDonald nutritional index (RMNI) has been used in several studies.6,11,12 It is calculated from serum albumin and serum transferrin:
RMNI5ð1:2·serum albuminÞ1ð0:013·serum transferrinÞ26:43:6;20 A zero or negative score indicates nutritional depletion. The RMNI has not been validated.6 The multi-question Mini Nutritional Assessment (MNA) has been shown to be reliable in assessing malnutrition in the geriatric population6,15,21 (Figure 1). The MNA includes questions on a variety of topics, such as anthropometric measures and dietary habits, which allows for a sophisticated measurement of malnourishment that takes into account multiple variables that affect nutritional status. A difference exists between screening nutritional tools and assessment tools. However, Ozkalkanli et al13 demonstrated that the odds ratio of the association between malnutrition
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Figure 1
The Mini Nutritional Assessment form. (Copyright Nestlé, 1994, Revision 2009.)
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Evaluation of Malnutrition in Orthopaedic Surgery
(ie, assessment tools) or the risk of malnutrition (ie, screening tools) and morbidity in orthopaedic surgery is 3.5 and 4.1, respectively. Thus, both types of tool can be used to predict increased morbidity following orthopaedic surgery. The World Health Organization classified obesity thus: class I, body mass index (BMI) 30.0 to 34.9 kg/m2; class II, BMI 35 to 39.9 kg/m2; and class III, BMI $40 kg/m2.22 The diagnostic criteria for DM are listed in Table 2.
Mechanisms for Malnutrition in Increasing Infection Risk Malnutrition is thought to predispose patients to SSI1,24-26 by impairing wound healing6,11,17 and prolonging inflammation via several mechanisms, including impaired fibroblast proliferation and collagen synthesis.27 Decreased lymphocyte count is thought to impair the ability of the immune system to eradicate or prevent infection. Obesity contributes to SSI by making it difficult to achieve adequate wound closure and through the process of fat necrosis, leading to impaired healing and the creation of dead space, which can lead to problems with local wound healing.27 Obesity is associated with increased surgical time, which further increases the risk of infection.28 DM predisposes patients to SSI by preventing the adequate utilization of glucose for energy and adequate oxygen delivery secondary to glycosylation of hemoglobin and micro- and macrovascular disease, which ultimately results in ischemic tissue that is more susceptible to infection.27
Malnutrition and SSI in Spine Surgery Both superficial and deep SSI after orthopaedic spinal surgery have been linked to several markers of malnu-
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trition, including serologic laboratory values, DM, hyperglycemia, and obesity.29-34 Because the risk of deep infection has been shown to be higher in patients with neuromuscular conditions, most research in spine surgery has been done to identify risk factors, including malnutrition, that may increase the risk of infection in this patient population. Whether poor preoperative nutrition as defined by serologic laboratory measurements increases the risk of deep infection after spinal surgery is a point of contention in the literature, however. Jevsevar and Karlin30 reported that preoperative albumin $3.5 mg/dL and total lymphocyte count $1,500 cells per cubic millimeter were associated with lower rates of overall infection in 44 patients with cerebral palsy after spinal surgery. Similarly, in a review of patients undergoing elective spine surgery, Beiner et al7 reported higher rates of postoperative infection and poor wound healing in patients with serum albumin levels ,3.5 mg/dL and total lymphocyte counts ,1,500 per cubic millimeter. Although most of the literature demonstrates an association between these serologic laboratory values and infection, a retrospective multicenter case-control study of 210 neuromuscular scoliosis surgeries found no statistically significant association between undernutrition, as defined by serum albumin ,3.5 mg/dL and total lymphocyte count ,1,500 per cubic millimeter, and increased risk of infection.31 In 2007, Friedman et al32 compared 41 cases of SSIs after laminectomy with 82 matched control subjects at a single site. Both DM and BMI .35 kg/m2 were found to be independent risk factors for SSI, with odds ratios of 4.2 and 7.1, respectively. In a case-control study published in 2008, 46 patients with SSI after spine surgery were compared with 227 uninfected control patients.33 Obesity
(ie, BMI of 30 to 35 kg/m2), DM, an elevated preoperative serum glucose level (.125 mg/dL), and postoperative serum glucose levels .200 mg/dL all were associated with increased risk of SSI. Thus, the risk of infection was higher even in patients who did not have a diagnosis of DM, which suggests that hyperglycemia and blood glucose impairment alone increase the risk of SSI, regardless whether the patient has a diagnosis of DM.4 A subsequent retrospective cohort analysis of 3,174 spinal surgeries at a single center corroborated these results by showing that DM was an independent risk factor for SSI and that obesity (BMI .30 kg/m2) increased the risk of superficial infection.34
Malnutrition and Total Joint Arthroplasty Malnutrition in several forms has been associated with increased risk of infection and impaired wound healing following total joint arthroplasty. Peersman et al24 retrospectively reviewed 6,489 total knee arthroplasties (TKAs) at a single site over 7 years and reported 97 prosthetic joint infections (PJIs). Compared with matched control patients, the factors of poor nutrition, obesity, and DM were found to increase the risk of PJI. Malnutrition has also been associated with persistent wound drainage and PJI.5 The impact of nutritional status on wound drainage and subsequent deep PJI was investigated in a retrospective review of 11,785 consecutive lower extremity arthroplasty procedures.1 Eighty-three patients had persistent wound drainage following irrigation and débridement and had further surgery. Of the patients who failed the additional surgical treatment and went on to develop deep infection, 35% were found to be undernourished (ie, serum albumin ,3.5 g/dL, total lymphocyte count ,1,500 per cubic millimeter, or transferrin
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Michael Brian Cross, MD, et al
Table 2 The Four Diagnostic Criteria for Diabetes Mellitus According to the American Diabetes Association23 Hemoglobin A1c $6.5% Fasting ($8 h) plasma glucose levels $126 mg/dL (or 7 mmol/L) Two-hour plasma glucose $200 mg/dL (11.1 mmol/L) during an oral glucose tolerance test Classic symptoms of hyperglycemia (eg, polydipsia, polyuria) or hyperglycemic crisis and random plasma glucose $200 mg/dL (11.1 mmol/L)
,200 mg/dL). The success rate of the initial irrigation and débridement in the malnourished population was only 5%. Font-Vizcarra et al8 prospectively studied 213 patients who underwent TKA and found malnutrition, as indicated by smaller triceps skinfold measurement, to be independently associated with both superficial and deep infection. Specifically, a triceps skinfold measurement of 30 mm was associated with a 5% risk of infection. The risk of infection was 10% with a skinfold measurement of 20 mm. The relationship between obesity and PJI has been studied extensively.24-26,28,35-37 In a prospective study of 1,509 consecutive TKAs, Chesney et al35 found that although morbid obesity (BMI .40 kg/m2) increased the odds for deep infection, it did not reach statistical significance. However, in a retrospective study, Peersman et al24 found that obesity significantly increased the risk of PJI. Similarly, in a retrospective review of 6,108 total hip arthroplasties (THAs) and TKAs, Malinzak et al28 found the odds for PJI to be 21.3 times greater in patients with BMI .50 kg/m2. The authors of a prospective study of 1,214 consecutive primary TKAs found that patients with morbid obesity (BMI $40 kg/m2) had a nine times greater risk of having a PJI after surgery compared with patients who were not obese.36 Diabetes combined with obesity further increased that risk. Patients with BMI of 30 to 39 kg/m2 were not at increased risk of infection. March 2014, Vol 22, No 3
In 2012, Bozic and colleagues published two separate analyses of the Medicare 5% claims database— one on TKA25 and the other on THA.26 The patient sample size was 83,011 in the TKA study and 40,919 in the THA study. In both studies, the diagnosis of obesity, which was filed in either inpatient or outpatient Medicare claims submitted during the 12 months before the operation, was found to be a statistically significant risk factor for PJI. Not all studies are definitive, however. In 2011, Davis et al37 published the results of a prospective study of 1,617 consecutive primary THAs performed in England. Although increased BMI (.35 kg/m2) was significantly associated with superficial infections, with an 89.5% increase in superficial infections per 10-point rise in BMI, it did not reach statistical significance for association with deep infection. However, this may have been due to the small number of deep infections in this series (15 total). Patients with obesity should be encouraged to lose weight and undergo a nutritional consultation before surgery. For patients with BMI .40 kg/m2, it is particularly important to assess baseline nutritional status and construct a meal plan designed for safe weight loss. Coexisting nutritional impairments should be corrected as well, including vitamin D deficiency, which is present in 80% to 90% of patients with obesity.4 Ensuring gradual, safe weight loss is important because rapid weight loss may cause undernourishment in some patients,34 which would simply replace one
nutritional disorder for another. Bariatric surgery may be an option before elective procedures because it may lessen the operative time, the anesthesia time, and the risk of perioperative complications; however, little has been published on this topic.38,39 The relationship between blood glucose impairment and DM and deep infections has been well-studied in the orthopaedic literature.25,26,28,35,36,40,41 Several studies have shown DM to be a risk factor for deep infection.25,26,28,35 Similarly, in a retrospective study, Jämsen et al40 reported that preoperative hyperglycemia (blood glucose level $110 mg/dL) was associated with higher risk of PJI. In 2009, Dowsey and Choong36 demonstrated that PJI occurred in patients with DM only if they had obesity. Thus, the authors postulated that there may be interaction between the two diseases, possibly involving the impact of obesity on blood glucose (ie, hyperglycemia). Although some studies demonstrate an increased risk of infection in patients with hemoglobin A1c .6.5%,42 a retrospective cohort study of 350 persons with diabetes and with varying degrees of DM control as measured by hemoglobin A1c level (,7% or $7%) found no statistically significant difference in incidence of SSI between the two groups.41
Summary and Clinical Recommendations Given the prevalence of malnutrition in orthopaedic patients and the impact
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Evaluation of Malnutrition in Orthopaedic Surgery
on the outcomes and complications of orthopaedic procedures, the surgeon should assess preoperative serum albumin level, total lymphocyte count, and transferrin level, and patients whose laboratory values fall below the cutoffs described above should undergo a nutritional consultation. Patients with DM should work to achieve improved glucose control, and they should be carefully monitored postoperatively. In our practice, we routinely obtain a hemoglobin A1c value preoperatively and discuss with the patient delaying elective surgery if that value exceeds 7%. Similarly, patients with obesity can attempt healthy weight loss with the help of a multidisciplinary team that includes a dietician, physical therapist, and internal medicine specialist. Unfortunately, medical insurance programs such as Medicaid do not cover such services. Although anthropometric measurements have been shown to be useful indicators of malnutrition in patients undergoing orthopaedic surgery,6,9,10 we do not recommend their use at this time because standardized cutoff values have not been established and because their use is not as well substantiated as use of serologic laboratory values. We do not recommend obtaining serum prealbumin levels because they are too sensitive to accurately reflect changes in protein-calorie nutrition.6 Standardized nutritional scoring systems that may be used as a substitute for serologic parameters include the RMNI,6,10,11 MNA,6,15 Nutritional Risk Screening 2002,13 and the subjective global assessment.13 If a patient is found to be malnourished, we recommend discussing with the patient the possibility of delaying elective surgery until the patient’s nutritional status has improved. To our knowledge, no study has shown improved outcomes as a result of correcting nutritional status preoperatively; however, given that the literature supports a link between
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malnutrition and increased morbidity after orthopaedic surgery, we believe that addressing malnutrition preoperatively is a reasonable approach in the attempt to reduce the risk of complications. Future studies should focus on whether improving preoperative nutritional status improves patient outcomes by decreasing the risk of morbidity after orthopaedic surgery.
nutritional status and post-operative infection in total knee replacements: A prospective study of 213 patients. Int J Artif Organs 2011;34(9):876-881. 9. Pratt WB, Veitch JM, McRoberts RL: Nutritional status of orthopedic patients with surgical complications. Clin Orthop Relat Res 1981;(155):81-84. 10. Jensen JE, Jensen TG, Smith TK, Johnston DA, Dudrick SJ: Nutrition in orthopaedic surgery. J Bone Joint Surg Am 1982;64(9):1263-1272. 11. Rai J, Gill SS, Kumar BR: The influence of preoperative nutritional status in wound healing after replacement arthroplasty. Orthopedics 2002;25(4):417-421.
References Evidence-based Medicine: Levels of evidence are described in the table of contents. In this article, references 8, 12-14, 17, 19, 24-26, 35-37, 40, and 41 are level II studies. References 1, 5, 6, 9, 10, 16, 28, 30-34, 39, and 42 are level III studies. References 11, 15, and 29 are level IV studies. Reference 27 is level V expert opinion. References printed in bold type are those published within the past 5 years. 1. Jaberi FM, Parvizi J, Haytmanek CT, Joshi A, Purtill J: Procrastination of wound drainage and malnutrition affect the outcome of joint arthroplasty. Clin Orthop Relat Res 2008;466(6):1368-1371. 2. Smith TK: Nutrition: Its relationship to orthopedic infections. Orthop Clin North Am 1991;22(3):373-377. 3. World Health Organization: WHO, Nutrition Experts Take Action on Malnutrition. Available at: http://www.who.int/nutrition/ pressnote_action_on_malnutrition/en/. Accessed December 17, 2013. 4. Via M: The malnutrition of obesity: Micronutrient deficiencies that promote diabetes. ISRN Endocrinol 2012;2012: 103472. 5. Greene KA, Wilde AH, Stulberg BN: Preoperative nutritional status of total joint patients: Relationship to postoperative wound complications. J Arthroplasty 1991; 6(4):321-325. 6. Guo JJ, Yang H, Qian H, Huang L, Guo Z, Tang T: The effects of different nutritional measurements on delayed wound healing after hip fracture in the elderly. J Surg Res 2010;159(1):503-508. 7. Beiner JM, Grauer J, Kwon BK, Vaccaro AR: Postoperative wound infections of the spine. Neurosurg Focus 2003;15(3):E14. 8. Font-Vizcarra L, Lozano L, Ríos J, Forga MT, Soriano A: Preoperative
12. Puskarich CL, Nelson CL, Nusbickel FR, Stroope HF: The use of two nutritional indicators in identifying long bone fracture patients who do and do not develop infections. J Orthop Res 1990;8(6): 799-803. 13. Ozkalkanli MY, Ozkalkanli DT, Katircioglu K, Savaci S: Comparison of tools for nutrition assessment and screening for predicting the development of complications in orthopedic surgery. Nutr Clin Pract 2009;24(2):274-280. 14. Zorrilla P, Gómez LA, Salido JA, Silva A, López-Alonso A: Low serum zinc level as a predictive factor of delayed wound healing in total hip replacement. Wound Repair Regen 2006;14(2):119-122. 15. Murphy MC, Brooks CN, New SA, Lumbers ML: The use of the MiniNutritional Assessment (MNA) tool in elderly orthopaedic patients. Eur J Clin Nutr 2000;54(7):555-562. 16. McPhee IB, Williams RP, Swanson CE: Factors influencing wound healing after surgery for metastatic disease of the spine. Spine (Phila Pa 1976) 1998;23(6):726-732, discussion 732-733. 17. Gherini S, Vaughn BK, Lombardi AV Jr, Mallory TH: Delayed wound healing and nutritional deficiencies after total hip arthroplasty. Clin Orthop Relat Res 1993; (293):188-195. 18. Beck FK, Rosenthal TC: Prealbumin: A marker for nutritional evaluation. Am Fam Physician 2002;65(8):1575-1578. 19. Cereda E, Pusani C, Limonta D, Vanotti A: The association of Geriatric Nutritional Risk Index and total lymphocyte count with short-term nutrition-related complications in institutionalised elderly. J Am Coll Nutr 2008;27(3):406-413. 20. Rainey-Macdonald CG, Holliday RL, Wells GA, Donner AP: Validity of a twovariable nutritional index for use in selecting candidates for nutritional support. JPEN J Parenter Enteral Nutr 1983;7(1):15-20.
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Michael Brian Cross, MD, et al 21. Guigoz Y: The Mini Nutritional Assessment (MNA) review of the literature: What does it tell us? J Nutr Health Aging 2006;10(6):466-485, discussion 485-487.
29. Li Y, Glotzbecker M, Hedequist D: Surgical site infection after pediatric spinal deformity surgery. Curr Rev Musculoskelet Med 2012; Feb 9 [Epub ahead of print].
22. World Health Organization: BMI Classification. Available at: http://apps. who.int/bmi/index.jsp?introPage=intro_3. html. Accessed January 13, 2014.
30. Jevsevar DS, Karlin LI: The relationship between preoperative nutritional status and complications after an operation for scoliosis in patients who have cerebral palsy. J Bone Joint Surg Am 1993;75(6):880-884.
23. American Diabetes Association: Diagnosis and classification of diabetes mellitus. Diabetes Care 2011;34(suppl 1):S62-S69. 24. Peersman G, Laskin R, Davis J, Peterson M: Infection in total knee replacement: A retrospective review of 6489 total knee replacements. Clin Orthop Relat Res 2001; (392):15-23. 25. Bozic KJ, Lau E, Kurtz S, Ong K, Berry DJ: Patient-related risk factors for postoperative mortality and periprosthetic joint infection in Medicare patients undergoing TKA. Clin Orthop Relat Res 2012;470(1):130-137. 26. Bozic KJ, Lau E, Kurtz S, et al: Patientrelated risk factors for periprosthetic joint infection and postoperative mortality following total hip arthroplasty in Medicare patients. J Bone Joint Surg Am 2012;94(9):794-800. 27. Seibert DJ: Pathophysiology of surgical site infection in total hip arthroplasty. Am J Infect Control 1999;27(6):536-542. 28. Malinzak RA, Ritter MA, Berend ME, Meding JB, Olberding EM, Davis KE: Morbidly obese, diabetic, younger, and unilateral joint arthroplasty patients have elevated total joint arthroplasty infection rates. J Arthroplasty 2009;24(6 suppl): 84-88.
31. Sponseller PD, LaPorte DM, Hungerford MW, Eck K, Bridwell KH, Lenke LG: Deep wound infections after neuromuscular scoliosis surgery: A multicenter study of risk factors and treatment outcomes. Spine (Phila Pa 1976) 2000;25(19):2461-2466. 32. Friedman ND, Sexton DJ, Connelly SM, Kaye KS: Risk factors for surgical site infection complicating laminectomy. Infect Control Hosp Epidemiol 2007;28(9): 1060-1065.
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Jämsen E, Nevalainen P, Kalliovalkama J, Moilanen T: Preoperative hyperglycemia predicts infected total knee replacement. Eur J Intern Med 2010;21(3):196-201.
33. Olsen MA, Nepple JJ, Riew KD, et al: Risk factors for surgical site infection following orthopaedic spinal operations. J Bone Joint Surg Am 2008;90(1):62-69. 34. Pull ter Gunne AF, Cohen DB: Incidence, prevalence, and analysis of risk factors for surgical site infection following adult spinal surgery. Spine (Phila Pa 1976) 2009;34 (13):1422-1428. 35. Chesney D, Sales J, Elton R, Brenkel IJ: Infection after knee arthroplasty: A prospective study of 1509 cases. J Arthroplasty 2008;23(3):355-359. 36. Dowsey MM, Choong PF: Obese diabetic patients are at substantial risk for deep infection after primary TKA. Clin Orthop Relat Res 2009;467(6):1577-1581.
Erratum Fresh Osteochondral Allograft Transplantation for the Knee: Current Concepts Seth L. Sherman, MD, Joseph Garrity, MS, Kathryn Bauer, James Cook, DVM, PhD, James Stannard, MD, and William Bugbee, MD (Vol 22, No 2, February 2014, pp 121-133) On the title page of this article, the MD degree was inadvertently deleted following Dr. Bauer’s name and, in the author notes, was incorrectly inserted after Mr. Garrity’s name. The byline should correctly read Seth L. Sherman, MD, Joseph Garrity, MS, Kathryn Bauer, MD, James Cook, DVM, PhD, James Stannard, MD, William Bugbee, MD. In the author notes near the bottom of the title page and in the disclosure paragraph at the bottom of the second article page, these authors’ names should read Mr. Garrity (rather than Dr. Garrity) and Dr. Bauer (rather than Ms. Bauer). The Journal regrets the error.
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