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RESEARCH PAPER Malnutrition and obesity: influence in mortality and readmissions in chronic obstructive pulmonary disease patients A. Zapatero,* R. Barba,† J. Ruiz,* J. E. Losa,‡ S. Plaza,§ J. Canora* & J. Marco¶ *Servicio de Medicina Interna, Hospital Universitario de Fuenlabrada, Madrid, Spain †Servicio de Medicina Interna, Hospital Rey Juan Carlos, Madrid, Spain ‡Servicio de Medicina Interna, Hospital Universitario Fundaci�on Alcorc�on, Madrid, Spain §Servicio de Medicina Interna, Hospital Severo Ochoa, Madrid, Spain ¶Servicio de Medicina Interna, Hospital Cl�ınico de San Carlos, Madrid, Spain Keywords COPD, malnutrition, mortality, obesity paradox, readmissions. Correspondence R. Barba, Hospital Rey Juan Carlos, Calle Gladiolo s/n nº 2, 28981 Parla, Madrid, Spain. Tel.: +349 1191 3555 Fax: +341 913 292 E-mail: raquel.barba@hospitalreyjuancarlos.es How to cite this article Zapatero A., Barba R., Ruiz J., Losa J.E., Plaza S., Canora J. & Marco J. (2013) Malnutrition and obesity: influence in mortality and readmissions in chronic obstructive pulmonary disease patients. J Hum Nutr Diet. doi:10.1111/jhn.12088 Abstract Background: The present study aimed to assess the association of obesity and malnutrition with the mortality of hospitalised patients with acute exac- erbation of chronic obstructive pulmonary disease (COPD) and the risk of readmission in <30 days. Methods: A retrospective chart review of consecutive patients admitted with COPD as the primary reason for discharge in Spain between 1 January 2006 and 31 December 2007 was performed. Patients with a diagnosis of obesity or malnutrition in the hospital discharge clinical report were identified. The in-hospital mortality and re-admittance 30 days after discharge indices of obese and malnourished patients were compared against the subpopulation without these diagnoses. Results: Of the 313 233 COPD admittances analysed, there were 22 582 (7.2%) diagnoses of obesity and 6354 (2.0%) diagnoses of malnutrition. In- hospital global mortality and the re-admittance risk were 12.0% and 16.7%, respectively. Obese patients showed a lower in-hospital mortality risk [odds ratio (OR) = 0.52; 95% confidence interval (CI) = 0.49–0.55] and early re- admittance risk (OR = 0.87; 95% CI = 0.85–0.92) compared to non-obese patients. Malnourished patients had a much higher risk of death when in hospital (OR = 1.73; 95% CI = 1.62–1.85) or of being re-admitted within 30 days after discharge (OR = 1.29; 95% CI = 1.22–1.38), even after adjust- ing for possible confounding factors. Conclusions: Obesity in patients hospitalised for COPD substantially reduces in-hospital mortality risk and the possibility of early re-admittance. Malnutrition is associated with an important increase in in-hospital mortal- ity and risk of re-admittance in the 30 days following discharge. Introduction Chronic obstructive pulmonary disease (COPD) is a major global health problem. It is the fourth-leading cause of death in the USA and is projected to be the third-leading cause of death worldwide by 2020 (Murray & Lopez, 1996; McGhan et al., 2007) affecting 4–9% of the adult population (Marti et al., 2006). Exacerbations of COPD disease comprise an important component of the burden of the disease by accelerating lung function decline, precipitating poor health status (Seemungal et al., 1998), increasing healthcare costs (Andersson et al., 2002) and negatively affecting survival (Connors et al., 1996) . Obesity is increasing dramatically throughout the Wes- tern world and is common in patients with COPD (Franssen et al., 2008; Ora et al., 2009). It is widely ª 2013 The British Dietetic Association Ltd. 1 Journal of Human Nutrition and Dietetics accepted that obesity in the general population is associ- ated with increased mortality and greater disease risk. However, in those who have experienced major illness or chronic disease, it appears that obesity is associated with improved survival. This ‘obesity paradox’ has been dem- onstrated in several recent studies of critically and chroni- cally ill patients, as well as in patients undergoing certain procedures, suggesting that overweight and obese patients may have better outcomes than normal weight patients (Fleischmann et al., 1999; Gurm et al., 2002; Kalantar- Zadeh et al., 2003; Lee et al., 2004; Marik, 2006; Fonarow et al., 2007; Barba et al., 2008; Mullen et al., 2009). Sev- eral studies have reported a significant effect of obesity on all-cause mortality in patients with severe COPD, with mortality being lowest in obese patients (Jee et al., 2006; Hallin et al., 2007; McGhan et al., 2007; Ora et al., 2009; Lainscak et al., 2011). Most of these studies have been carried out in a community-based setting. By contrast, weight loss, a low body mass index (BMI) and cachexia have important negative prognostic implica- tions in patients with COPD (Landbo et al., 1999; Chail- leux et al., 2003). The role of low BMI in these patients could have been related to several factors, such as respira- tory muscle weakness, impaired gas exchange and an impaired immune response (Landbo et al., 1999). The present study aimed to assess the association of obesity and malnutrition with the mortality of hospita- lised patients with acute exacerbation of COPD and the risk of readmission in <30 days for the same process. Materials and methods The present study included all patients who were admit- ted to all acute care hospitals of the Spanish Public Health Service through an emergency department between 1 January 2006 and 31 December 2007 with COPD as the primary reason for discharge. All elective admissions and elective transfers were excluded. Hospital discharge data were obtained from the Basic Minimum Data Set (BMDS). BMDS contains sociodemographic and clinical data for each documented hospital stay, including sex and age, primary and secondary diagnoses [according to the International Classification of Diseases, Ninth Revi- sion, Clinical Modification (ICD-9-CM) code]; primary and secondary procedures; admission and discharge sta- tus; length of stay; and hospital characteristics (group 1: <150 beds; group 2: 150–200 beds, group 3: 200–500 beds; group 4: 500–1000 beds; group 5: >1000 beds). For every patient, a diagnosis-related group (DRG) was iden- tified. DRGs are a method of classifying patient hospitali- sations by diagnosis and procedure on the assumption that similar costs are expended on patients by using simi- lar resources. The CMBD registry is compulsory for every patient admitted to a hospital of the Spanish National Health Service, a system that cares for >90% of the coun- try’s population. Cases were selected if they were discharged with the diagnosis of COPD (code DRG 88: Chronic Obstructive Pulmonary Disease; 540: Respiratory infections & inflam- mations with major complications; or 541: Respiratory disorders except infections, bronchitis, asthma with major complications; DRG-AP.21 version). The primary diagno- sis of COPD was identified using ICD-9-MC codes in the primary diagnosis field: 491.0, 491.1, 491.9, 491.20, 491.21, 491.22, 496, 518.8, 518.81 and 518.9. The standardised definition of the variable readmission in the Spanish CMBD has been defined as a new hospital- isation in the following month with the same major diag- nostic category in the main diagnosis. The patients who had a secondary diagnosis of obesity (ICD-9-CM: 278.00–278.02) or malnutrition (ICD-9-CM: 260–263.9) were analysed. The age adjusted Charlson Co-morbidity Index (CCI) was computed for each patient. This index reflects the number and importance of comorbid diseases, relieson ICD-9-CM categories, and was used to adequately adjust for severity of illness (Charlson et al., 1987; Deyo et al., 1992). The following risk factors were identified using ICD-9- MC codes in any primary or secondary diagnosis field: cardiac disease: ICD-9-MC: 398.91, 404*, 402.11, 402.91,428–428.9; dementia: ICD-9-MC: 290–290.9; cancer ICD-9-MC: 140.0–172.9, 174.0–195.8, 200–208.9, V10.0– V10.9; diabetes: ICD-9-CM: 250.00–250.99; chronic renal failure: ICD-9-CM: 585–586.99, 582.0–582.9, 583.0–583.7, 588.0–588.9; hypertension: ICD-9-CM: 401.0, 401.1, 401.9; anaemia: ICD-9-CM: 280.00–285.99; tobacco: ICD-9-CM: 305.10; atrial fibrillation: ICD-9-CM: 427.3–427.32. The following acute medical illness were considered when they occurred during the index hospitalisation, and then only primary diagnoses ICD-9-MC codes were used: acute con- gestive heart failure: ICD-9-MC: 398.91, 404*, 402.11, 402.91,428–428.9; acute renal failure: ICD-9-MC: 403.11, 403.91,404.12, 585–586; acute respiratory failure: ICD-9- MC: 518.81–518.84; acute infectious disease: ICD-9-MC: 001–137, 460–466, 487–487.8; and cerebrovascular disease: ICD-9-MC: 430–438. The present study was approved by the Ethics Commit- tee in Infanta Cristina Hospital, Parla, Madrid, Spain. Statistical analysis A descriptive analysis of these patients was carried out, and the demographic variables among the patients diag- nosed with or without malnutrition, and with or without obesity, were compared. We used the chi-squared test for 2 ª 2013 The British Dietetic Association Ltd. Malnutrition and obesity in COPD A. Zapatero et al. categorical variables with Yates correction, Fisher’s exact test for dichotomous variables when the expected value of a cell was <5, and Student’s t-test or analysis of variance for quantitative variables. All univariate analyses were car- ried out after adjusting for age and sex. Odds ratios (OR) and 95% confidence intervals (CI) were estimated from the regression coefficients. Because this is an administrative database, the control of the confounding variables is basic. For this reason, a multivariate logistic regression analysis was carried out with the aim of determining the excess of mortality attributable to malnutrition or obesity, after correction of possible confounding variables such as the age of the patient (in years, as a continuous variable), Charlson index (in points, as a continuous variable), sex and all variables that had demonstrated a statistically significant relation in the univariate analysis with mortality [length of stay (days, continuous variable), cancer, dementia, heart failure, acute respiratory failure and smoking]. We also used multivariable logistic regression analysis to measure the independent association of the following factors with early readmission to hospital: sex, length of stay, age, cancer, dementia, heart failure, acute respira- tory failure, smoking, obesity and malnutrition. A logis- tic regression analysis with backward stepwise procedure and P > 0.10 as the criterion for exclusion, was used to find the best predictive models. Stratified analyses were performed to examine confounders and interactions where appropriate. All statistical analyses were carried out using SPSS, version 16 (SPSS Inc., Chicago, IL, USA). Results During the study period, there were 313 233 patient dis- charges with acute exacerbation of COPD. The median (SD) age of patients was 73.92 (12.97) years; 70.3% of the patients were men. The median (SD) stay was 10.75 (9.18) days. A CCI � 2 was present in 22.8% of the cases. A total of 22 582 (7.2%) subjects were obese, and 6354 (2%) were diagnosed with some form of mal- nutrition. The main characteristics of our subjects are shown in Table 1. Obese patients were more frequently women (40.8% versus 29.4%; P < 0.001), younger (70.3 versus 72.8 years; P < 0.001) and there was a greater proportion of smokers (17.8% versus 14.0%; P < 0.001) than in non-obese patients. On the other hand, malnourished patients were older (75.3 versus 72.8%; P < 0.001), fewer were smokers (12.1% versus 14%; P < 0.0001) than normoweight patients, and they were more frequently women (36.5% versus 29.4%; P < 0.001). Co-morbid conditions were common in our cohort, with hypertension, heart failure, diabetes, cancer and dementia in 31.4%, 17.3% 22.8%, 12.3% and 5.6% of the overall cohort, respectively. Cancer and dementia was more prevalent among patients with malnutrition, with unadjusted ORs in the presence of malnutrition compared to its absence for cancer (OR = 1.13; 95% CI = 1.05– 1.21), for dementia (OR = 3.68; 95% CI = 3.47–3.94). On the other hand, these conditions were less prevalent among patients with obesity (cancer: OR = 0.37; 95% CI = 0.35–0.39; dementia: OR = 0.35; 95% CI = 0.32– 0.38) compared to its absence. Obese patients more frequently suffer hypertension, diabetes and acute respira- tory failure than non-obese or malnourished patients (Table 1). Of the 313 233 patients, 37 718 died during admission (12%) and 52 428 (16.7%) were readmitted at least once within 30 days of the index date of admission with the same Major Diagnostic Category as the main diagnosis. Malnutrition was related to risk for death (unadjusted OR = 2.15; 95% CI = 2.02–2.29) and readmission (unad- justed OR = 1.41; 95% CI = 1.32–1.50), whereas obesity behaved as a protector factor for both (unadjusted OR for death = 0.41; 95% CI = 0.38–0.44) and unadjusted OR for readmission = 0.81; 95% CI = 0.77–0.84) (Table 2). The lowest risk of readmission and mortality was linked to a diagnosis of obesity. The association between obesity in COPD patients and readmission (OR = 0.87; 95% CI = 0.84–0.91) remained significant after adjusting for possible confounders such as cancer, heart failure, age, length of stay, sex, smoking or acute respiratory fail- ure. Obese patients had a 51% reduction in the risk of mortality (OR = 0.49; 95% = CI 0.46–0.53) after adjust- ing for possible confounders (Tables 3 and 4). Compared to normal weight, the risk of readmission within 30 days in COPD patients is 29% higher if malnu- trition is documented in medical chart (OR = 1.29; 95% CI = 1.21–1.37), and the risk of death is 77% higher, after adjusting for other variables that were significantly related to mortality in the univariate analyses (OR = 1.77; 95% CI = 1.65–1.89) (Tables 3 and 4). Discussion The present study describes the clinical outcomes of a large cohort of patients after hospitalisation for a severe exacerbation of COPD. We found that approximately 7% of patients hospitalised for COPD had a diagnosis in their clinical chart of obesity and 2% had a diagnosis of mal- nutrition. Compared to normal weight patients, the risk of readmission within 30 days after discharge in patients with a diagnosis of COPD is 13% lower if obese and 29% higher if malnutrition is documented in their medical chart. We also have observed that obese patients with ª 2013 The British Dietetic Association Ltd. 3 A. Zapatero et al. Malnutrition and obesity in COPD COPD have an almost 50% lower risk of death during hospitalisation than patients with normal weight and also that malnutrition is an important predictor of a poor outcome, with a 77% in-hospital mortality increase. Landbo et al. (1999) , were the first to examine the relation between BMI and mortality in patients with COPD. Their study, based on a large, nonselected, pro- spectively examined population with a long follow-up, demonstrated that BMI had an independent effect on all- causes of mortality both in men and women with severe COPD, with the lowest risk occurring in normal weight to overweight subjects and thatmortality decreased with increasing BMI (Landbo et al., 1999) Lainscak et al. (2011) analysed the association between BMI and mor- tality in COPD in a retrospective survey including patients hospitalised for acute exacerbation of COPD and found that the optimal BMI with the lowest risk of death was in the overweight category (BMI of 25.09– 26.56 kg m–2). In another study conducted in European Nordic countries in hospitalised patients with COPD, Hallin et al. (2007) found that the lowest mortality was among overweight patients, whereas being underweight was related to an increase in overall mortality. The associ- ation between being underweight and mortality in COPD Table 1 Characteristics of the patients in the study cohort Normal-weight (n = 284 297) Obese (n = 22 582) Malnutrition (n = 6354) P Age (years), mean (SD) 72.8 (15.9) 70.3 (11.9) 75.3 (17.4) <0.0001 Sex (men), mean (SD) 200 841 (70.6) 13 336 (59.2) 4036 (63.5) <0.001 Length of stay (days), mean (range) 9.7 (0–443) 9.6 (0–368) 15.9 (0–300) <0.001 Death, n (%) 35 009 (12.3) 1292 (5.7) 1417 (22.2) <0.001 Readmission, n (%) 47 840 (16.8) 3191 (14.1) 1397 (22.0) <0.001 Tobacco, n (%) 39 822 (14.0) 4025 (17.8) 772 (12.1) <0.001 Diabetes, n (%) 61 581 (21.7) 8703 (38.5) 1126 (17.7) <0.001 Hypertension, n (%) 87 008 (30.6) 9849 (43.6) 1360 (21.4) <0.001 Heart failure, n (%) 47 399 (16.7) 5951 (26.4) 917 (14.4) <0.001 Acute respiratory failure, n (%) 148 779 (52.3) 13 531 (59.9) 3328 (52.4)* <0.001 Cancer, n (%) 36 433 (12.8) 1194 (5.3) 845 (13.3)* <0.001 Dementia, n (%) 16 093 (5.7) 436 (1.2) 1158 (18.2) <0.001 *P = not significant when malnutrition/normal weight is compared. Table 2 Unadjusted analysis: association between mortality and readmission with obesity and malnutrition in chronic obstructive pulmonary disease patients Odds ratio (95% confidence interval) Obese patients Mortality 0.41 (0.38–0.44) Readmission 0.81 (0.77–0.84) Malnourished patients Mortality 2.15 (2.02–2.29) Readmission 1.41 (1.32–1.50) Patients were considered for inclusion in the obesity and malnutrition group if they have a diagnosis included in the hospital discharge report. Table 3 Risk factors for mortality during admission in the chronic obstructive pulmonary disease cohort (multivariate regression analysis) Odds ratio 95% confidence interval P Sex (male) 1.211 1.182 1.242 <0.001 Length of stay (days) 1.004 1.003 1.005 <0.001 Age (years) 1.030 1.029 1.031 <0.001 Cancer 4.641 4.487 4.800 <0.001 Dementia 2.347 2.259 2.440 <0.001 Heart failure 1.184 1.148 1.221 <0.001 Acute respiratory failure 2.248 2.194 2.303 <0.001 Charlson index 1.024 1.015 1.033 <0.001 Tobacco 0.696 0.667 0.727 <0.001 Obesity 0.494 0.465 0.525 <0.001 Malnutrition 1.767 1.651 1.890 <0.001 Table 4 Risk factors for 30-day readmission in the chronic obstructive pulmonary disease cohort (multivariate regression analysis) Odds ratio 95% confidence interval P Sex (male) 0.752 0.729 0.774 <0.0001 Length of stay (days) 1.013 1.011 1.022 <0.0001 Age (years) 1.001 1.000 1.001 0.010 Cancer 1.538 1.486 1.580 <0.0001 Dementia 1.010 0.960 1.051 0.761 Heart failure 1.082 1.055 1.119 <0.0001 Acute respiratory failure 0.997 0.978 1.016 0.222 Charlson index 1.204 1.176 1.232 <0.0001 Tobacco 0.792 0.778 0.827 <0.0001 Obesity 0.870 0.846 0.915 <0.0001 Malnutrition 1.290 1.218 1.376 <0.0001 4 ª 2013 The British Dietetic Association Ltd. Malnutrition and obesity in COPD A. Zapatero et al. patients remained significant after adjusting for possible confounders such as forced expiratory volume in the first second (FEV1). For COPD, several scoring systems for predicting prog- nosis have been developed. The BODE composite score is the most frequently used in everyday practice. Although it is primarily limited to patients with clinically stable disease as seen in an outpatient setting, this score includes body mass index, the degree of airflow obstruction, dyspnea and exercise capacity (E; Celli et al., 2004). The authors found that BMI values <21 were associated with an increased risk of death, which is an observation similar to that reported by Landbo et al. (1999) in a large population study. The mechanisms underlying the above-mentioned find- ings on the obesity paradox remain unresolved. Why does obesity paradoxically improve survival in patients with COPD and why is a higher BMI associated with fewer respiratory-related deaths? Ora et al. (2009) recently explored the relationship between obesity, operating lung volumes and exercise intolerance in patients with moder- ate to severe COPD. By contrast to current beliefs, the combination of obesity and COPD was not associated with diminished exercise capacity or greater dyspnea compared to normal weight patients with a similar reduc- tion in FEV1. The explanation could be that the presence of airway obstruction does not alter the relationship between increasing BMI and lung volumes (expiratory reserve volume and functional residual capacity) seen in healthy populations (Deesomchok et al., 2010). In other words, these lung volume components also decrease exponentially as BMI increases in patients with COPD. Obese COPD patients consistently demonstrate less lung hyperinflation and have a larger inspiratory capacity and inspiratory capacity/total lung capacity ratio than their lean counterparts matched for FEV1 (Ora et al., 2009). Guenette et al.(2010) concludes that a fundamental question is whether the reported benefits of an increased BMI in this population are derived from an increased fat- free skeletal muscle mass, from the effects of excessive adipose tissue on the mechanics of the respiratory system, or from some combination of both. The contribution of abdominal fat mass to systemic inflammation often pres- ent in COPD has been demonstrated in different studies, although the precise mechanism and significance of the associations between adipokines and lung disease at the current moment is confusing, and needs further investiga- tion (Breyer et al., 2009; Rutten et al., 2010; Sood, 2010). Prospective longitudinal studies that examine the interac- tion of changes in body composition and the temporal progression of pulmonary function decline (after control- ling for the relevant comorbidities) are needed to better understand this intriguing relationship between increased BMI and survival in COPD populations. Malnutrition is a well known complication of COPD (Chailleux et al., 2003). It is clear that being underweight or having a low fat-free mass is associated with poor sur- vival in COPD (Celli et al., 2004; Tsimogianni et al., 2009) independently of the degree of airway obstruction (Landbo et al., 1999), even in patients receiving long- term oxygen therapy (Chailleux et al., 2003; Marti et al., 2006). Furthermore, a decrease in fat mass has recently been identified as an independent risk factor for mortality in COPD patients, regardless of the fat mass (Schols et al., 2005). Hence, protein depletion may be a negative feature in the prognosis of these patients, even though their weight is normal (Marti et al., 2006). Nutritional assessment should be included in the initial evaluation of all patients and the diagnosis of malnutri- tion/undernourishment in discharge reports (Landbo et al., 1999; Hallin et al., 2007; Lainscak et al., 2011); however, malnutrition is systematically underdiagnosed, and therefore a long way from being corrected. The work of nurses or dietitians is important in this field and could represent an invaluable tool for improving the quality of care given to the patients admitted to our departments.It is also necessary for foodservices to be recognised as a clinical and not corporate or ‘hotel’ activity. Hospital information systems constitute fundamental tools for clinical management (Marco et al., 2011) but, on many occasions, the diagnosis of malnutrition is not reflected in discharge sheets. Whether rectifying nutritional status with directed efforts at nutritional support or whether malnutrition would resolve with more intensive COPD care remains unclear (Ferreira et al., 2005). However, given the means available to correct malnutrition, prospective interven- tional studies (such as evaluating the effects of different COPD therapies on nutritional parameters or improving nutrition in these patients) are warranted. Some potential limitations of the present study deserve comment, particularly when using administrative data. A large proportion of patients hospitalised with the diagno- sis of COPD have never had a confirmatory test, includ- ing those with presumably advanced disease. Compared to patients with chronic heart failure, patients with COPD are less likely to have had the confirmatory test performed, even when both conditions coexist (Damarla et al., 2006). In the present study we do not have the BMI stage and, similarly, we know that both the diagnosis of obesity and malnutrition may be underdiagnosed (Marco et al., 2011). On the other hand, we have been able to provide a very large series of patients (>300 000) comprising all COPD patients admitted to the internal medicine departments of Spanish hospitals for a consecu- tive period of 2 years with all its associated statistical power. ª 2013 The British Dietetic Association Ltd. 5 A. Zapatero et al. Malnutrition and obesity in COPD On the basis of the present study of subjects with COPD, utilising a unique database from an integrated health care system, we conclude that obesity appears to be associated with an important reduction in mortality during admis- sions for acute exacerbations of COPD and a reduction in the risk of readmission. Similarly, malnutrition could be an important independent factor for mortality and rehospital- isation in the next 30 days. Further studies are needed to show whether identifying and treating weight loss could act towards improving the prognosis for hospitalised COPD patients. Additionally the obesity paradox is a complex phenomenon that requires additional investigation, and future studies should consider weight change when evaluat- ing the longitudinal association among health, overweight/ obesity and outcomes. Acknowledgments The authors thank the Spanish Minister of Health for the permission to obtain of the data. Conflicts of interest, sources of funding and authorship The authors declare that there are no conflicts of interest. No funding was received for the conduct and interpreta- tion of these analyses. RB conceived the study, performed the statistical analy- sis and analysed the results. AZ was the coordinator of the group and, as president of the Group of Medical Management of the SEMI (Sociedad Espa~nola de Medi- cina Interna–Spanish Society of Internal Medicine), acted as the official liaison with the Spanish Ministry of Health for the procurement of the crude data. JR car- ried out the bibliographic revision. JM wrote the first draft of the paper, as well as its final version, for the approval of the other authors. SP helped to obtain meaning from the raw data. JEL performed all the perti- nent crosses between the partial results to achieve the statistically significant final results. JC helped to write the discussion of the paper and carried out the biblio- graphic revision. All authors contributed to the design and conduct of the study and read and approved the final manuscript submitted for publication. References Andersson, F., Borg, S., Jansson, S.A., Jonsson, A.C., Ericsson, A., Prutz, C., Ronmark, E. & Lundback, B. 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