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doi:10.1111/jpc.12888
ORIGINAL ARTICLE
Clinical audit results in earlier nutritional intervention in malnourished children with cystic fibrosis with improved outcome Oren Ledder,1 Mark R Oliver,1,2,3 Ralf G Heine,1,2,3 Joanne Graham,4 Evelyn Volders5 and Philip J Robinson2,3,4 Departments of 1Gastroenterology and Clinical Nutrition and 4Respiratory Medicine, Royal Children’s Hospital, 2Department of Paediatrics, University of Melbourne, 3Murdoch Childrens Research Institute, and 5Department of Nutrition & Dietetics, Monash University, Melbourne, Victoria, Australia
Aim: The association between nutritional status, pulmonary function and survival in cystic fibrosis (CF) is well established. A previous case series from the Royal Children’s Hospital, Melbourne (RCH), demonstrated suboptimal referral practices and highlighted the importance of early nutritional interventions in children with CF. Various qualitative changes were made to our CF service, and this study assesses the effects of these practice changes timing of gastrostomy and clinical outcome in patients who underwent gastrostomy insertion. Method: Clinical audit of all CF patients who had undergone gastrostomy insertion from 2002 to 2010 at Royal Children’s Hospital. Clinical data, including nutritional parameters, respiratory function and survival, were collected at 2 years prior and 2 years post gastrostomy insertion. Data were compared with the previous study from 1989 to 1997. Results: Patients with CF who underwent gastrostomy insertion between 2002 and 2010 (n = 22) had higher weight-for-age scores (−1.5 ± 0.68 vs. −2.67 ± 1.06; P = 0.0001) and higher forced expiratory volume in 1 s (68% ± 22 vs. 52% ± 18.5; P = 0.006), compared with the cohort from 1989 to 1997 (n = 37). These differences were maintained at 2-year follow-up. Pseudomonas aeruginosa colonisation rate was 100% in 1989–1997 vs. 41% in 2002–2010; P = 0.0001. The 2-year survival post-gastrostomy insertion improved from 70% to 100%; P = 0.004. Conclusion: Earlier referral of patients in the recent cohort resulted in sustained improvements in weight-for-age and lung function. Survival at 2 years post-procedure was significantly improved. This study confirms the value of clinical audits and subsequent re-evaluation of clinical services. Key words:
gastroenterology; nutrition, respiratory.
What is already known on this topic
What this paper adds
1 Aggressive nutritional support is associated with improved outcomes in malnourished patients with cystic fibrosis (CF) and has been shown to improve lung function, as well as overall survival. 2 A structured, multidisciplinary CF clinic leads to improved patient care and better outcomes. 3 Quality audits are a critical component in continuously improving clinical service.
1 Close involvement of nutrition and gastroenterological services in a multidisciplinary CF clinic aids in the early detection of malnutrition in CF patients and facilitates insertion of gastrostomy at a more timely stage. 2 More timely insertion of a gastrostomy in malnourished CF patients contributes positively to better growth, lung function and possibly survival. 3 Quality audit directed implementation of clinical practice changes should be re-evaluated with repeat audits to verify outcomes (closing the audit-loop).
The close association between nutritional status, pulmonary function and survival in cystic fibrosis (CF) is generally accepted.1–4 Children and adolescents with advanced CF are often unable to meet their rapidly increasing energy requirements.5 Anorexia associated with chronic lung infection, nutrient maldigestion and malabsorption, gastro-oesophageal reflux Correspondence: Dr Mark R Oliver, Department of Gastroenterology and Clinical Nutrition, Royal Children’s Hospital, Flemington Road, Parkville, Vic. 3052, Australia. Fax: +61·39345 6240; email: [email protected] Conflict of interest: None. Accepted for publication 2 March 2015.
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disease and glucosuria, among others, are important factors leading to the development of malnutrition.6 Furthermore, a high total body muscle turnover predisposes patients with CF to respiratory muscle wasting which, in turn, may accelerate the progression of lung disease.7 Successful nutritional programmes have recognised the need to address not only these physiological factors, but also the psychosocial circumstances contributing to malnutrition.8 Such programmes have reduced the prevalence of nutritional deficiency states and protein-energy malnutrition.9 Some malnourished patients fail to respond to intensive multidisciplinary support such as education, dietary advice, optimisation of pancreatic replacement therapy and intensive
Journal of Paediatrics and Child Health 51 (2015) 988–993 © 2015 The Authors Journal of Paediatrics and Child Health © 2015 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
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treatment of pulmonary exacerbations.10 For these patients, the US CF Foundation recommends early intervention with aggressive nutritional supplementation via nasogastric or gastrostomy feeding.11 Long-term nutritional rehabilitation by gastrostomy has been shown to significantly improve weight, height and body mass index (BMI) z-scores and may ameliorate the progression of the pulmonary disease.12–17 Clinical care is provided for over 300 children with CF at the Royal Children’s Hospital in Melbourne (RCH). A previous study at RCH in children with CF demonstrated suboptimal referral practices and supported the importance of early nutritional intervention, such as supplemental feeds, pancreatic enzyme replacement optimisation and referral for gastrostomy insertion.18 As a result of this review, an additional full-time dietitian was appointed in 2002, and second-monthly rather than third-monthly outpatient visits were instituted in an attempt to facilitate a more aggressive approach to nutritional care of the patients. A further change included improved cohorting of patients according their pulmonary colonisation status. This retrospective study was primarily aimed at assessing whether improved dietetic and clinical follow-up impacted on the referral pattern of our patients from the pulmonologists (who provide the majority of the primary care of these patients) to the gastroenterology service. We also aimed to see if this led to better clinical outcomes in terms of weight gain and lung function. We therefore conducted a second clinical audit, comparing our current CF cohort to our previously published cohort of 37 patients with CF.18
Methods We conducted a retrospective clinical audit of all patients with CF at RCH who required gastrostomy insertion for nutritional management between 2002 and 2010. This clinical audit was approved by the Ethics in Human Research Committee at the Royal Children’s Hospital, Melbourne. We retrieved data for patients with CF who received gastrostomy feeds between 1989 and 1997, whom we had previously studied, and compared these with the current cohort.18 The diagnosis of CF was confirmed in all patients on the basis of clinical manifestations and abnormal sweat chloride. All patients were pancreatic insufficient, as demonstrated by either an abnormal 3-day faecal fat balance, or the presence of fat globules on faecal microscopy, in conjunction with a clinical history of steatorrhoea. Children with persistent poor weight gain were assessed for nutritional intake, and other causes for poor weight gain, such as diabetes mellitus or coeliac disease, were excluded on clinical and laboratory grounds. Adherence to pancreatic enzyme therapy was closely monitored during this period. Proton pump inhibitors were prescribed for a period of 3–6 months as an adjunct therapy to aid fat absorption, as per Australian CF guidelines on pancreatic enzyme replacement therapy.19 Prior to gastrostomy insertion, patients were closely monitored by our multidisciplinary team that included a pulmonologist, gastroenterologist, dietitian and clinical psychologist. Patients were provided with printed information regarding gastrostomy and enteral feeds. Gastrostomy insertion was recommended in the current group by consensus of the treating pulmonologist, gastroenterologist and dietitian if weight loss was greater than 2 bands on the
Gastrostomy feeding in paediatric CF
growth chart or if there was lack of improvement in children to reach the target BMI 10–25th percentile after a 3- to 6-month period of intensive dietary counselling and oral energy supplementation.17 After gastrostomy insertion, patients were asked to use their gastrostomy tube for supplemental feeding on five to six nights per week. Patients were prescribed dietary supplements providing 30–40 kcal/kg (125–170 kJ/kg) per day, which were administered by continuous overnight infusion. Pancreatic enzymes were administered at the commencement and completion of gastrostomy feeds. This feeding protocol utilised a standard nutritionally balanced polymeric formula with scope for different manufacturers and brands as per preference or availability. Ongoing assessment of compliance was assessed during regular 2nd–3rd monthly clinic reviews with both the treating physician and the dietician. All costs of nutritional supplementation were covered by a state government programme, effectively neutralising the cost burden of supplemental formula to assist compliance regardless of socio-economic circumstances. Weight, height and respiratory function tests were measured during the period 2 years before and after gastrostomy insertion in both cohorts. The best achieved spirometry measurements at each time point was recorded and used for the data comparisons between the two cohorts. Colonisation rates with Pseudomonas aeruginosa and 2-year survival were also recorded. Data for the 1989–1997 cohort was re-analysed using the current statistical methods (rather than weighted means that we used in the previously analysis). Standard deviation scores (z-scores) for weight-for-age (WAZ) and height-for-age (HAZ) were calculated using the epidemiological software program Epi Info 2000 (Centers for Disease Control and Prevention, Atlanta, GA, USA).20 Spirometry measurements were obtained from all patients 5 years and older, and the forced expiratory volume in 1 second (FEV1) was expressed as percentage predicted, after adjusting for weight, height and gender.21 Comparisons of growth and lung function data were made between the cohorts of 2002–2010 and 1989–1997. The study was divided into five time points (i.e. 2 years before, 1 year before, at time of insertion, 1 year post-gastrostomy insertion and 2 years postgastrostomy insertion).
Data analysis Normally distributed data were presented as mean ± standard deviation, or as median and interquartile range for skewed data. Anthropometric and lung function data at a time point in both cohorts were compared with each other using the unpaired two-sample t-test. To assess changes in lung function and anthropometric data within each cohort over time, a repeated measure analysis of variance was used. Fisher’s exact test was used to assess rates of survival and colonisation with P. aeruginosa. All data analyses were performed using GraphPad Prism 5 software (GraphPad Software, Inc. La Jolla, CA, USA).
Results Characteristics of the 2002–2010 cohort Between 2002 and 2010, 22 patients (mean age 9.7 ± 2.7 years; 12 female (54.5%) ) with CF underwent gastrostomy insertion
Journal of Paediatrics and Child Health 51 (2015) 988–993 © 2015 The Authors Journal of Paediatrics and Child Health © 2015 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
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in order to improve their nutritional status. All children were pancreatic insufficient. Fifty-eight per cent of children were homozygous, and 33% were heterozygous for ΔF508 deletion. One child was below the age of 5 years at the time of gastrostomy insertion and was unable to perform lung function tests. Nine patients were colonised with P. aeruginosa and two had CF-related diabetes mellitus at the time of insertion. No patient died during the 2-year follow-up period.
Characteristics of the 1989–1997 cohort There were 37 patients (mean age 11.6 ± 4.8 years, 15 female (40.5%) ). All were pancreatic insufficient and colonised with P. aeruginosa. Fifty-six per cent of children were homozygous and 22% were heterozygous for ΔF508 deletion. Eleven patients (seven female (64.6%)) died during the 2-year follow-up, with a median survival of 0.91 years (interquartile range 0.18–1.26).
Comparison of data for cohort from 1989–1997 and 2002–2010 The mean age at the time of gastrostomy insertion was similar for both cohorts (11.6 years ± 4.8 vs. 9.7 years ± 2.7; P = 0.14). The cohort of 1989–1997 had significantly lower WAZ scores at gastrostomy insertion (WAZ −2.67 ± 1.06 vs. −1.53 ± 0.68; P = 0.0001). Lung function was also significantly lower for the earlier cohort (FEV1 52% ± 18.5 vs. 68% ± 22; P = 0.006). There were no substantial differences in HAZ scores between cohorts. Gastrostomy insertion occurred at a substantially higher BMI centile in the recent cohort, compared with the original group
Table 1 Comparison of patient characteristics at the time of gastrostomy insertion between both cohorts
Number of patients Mean age (SD) at insertion Gender (M:F) WAZ score HAZ score FEV1 (% predicted) P. aeruginosa positive (n (%) ) Survival 2 years post PEG (n (%) )
1989–1997
2002–2010
P value
37 11.6 (±4.8) 1.47 : 1 −2.67 (±1.06) −1.41 (±1.02) 52 (±18) 37 (100) 26 (70)
22 9.7 (±2.7) 0.83 : 1 −1.53 (±0.68) −1.06 (±0.76) 68 (±22) 9 (41) 100%
0.14 0.42 0.0001 0.17 0.006 0.0001 0.004
(19.5 ± 16.2 vs. 3.4 ± 6.9; P = 0.0001). There was a dramatic reduction in pulmonary colonisation rates with P. aeruginosa from 100% in the previous cohort to 41% in the current group (P = 0.0001). The 2-year survival was 70% in the earlier cohort and 100% in the recent cohort (P = 0.004) (Table 1). Anthropometric and lung function data for both cohorts were compared between the time of insertion and four other time points: −2, −1, +1 and +2 years (Table 2). For weight (WAZ), there were significant differences at all four time points (Fig. 1). For the 2002–2010 cohort, WAZ improved from −1.53 ± 0.68 at insertion to −1.0 ± 0.68 at +2 years; P = 0.01. For the 1989–1997 cohort, the increase in WAZ was not significant (WAZ −2.67 ± 1.06 at insertion vs. −2.48 ± 1.55 at +2 years; N.S.). With respect to height (HAZ), data are summarised in Figure 2. There were no significant differences at any time point between the two cohorts. For FEV1, there were significant differences at all the time points (Fig. 3). Mean FEV1 in the 2002–2010 cohort fell from 81.8% ± 21 (n = 19) at –2 years to 68% ± 22 (n = 21) at insertion (P = 0.07) and remained stable at +2 years (68% ± 19 (n = 22) ). For the 1989–1997 cohort, a similar pattern was observed (Fig. 3). Of note, one child in each cohort had their gastrostomy removed after demonstrating persistent successful weight gain and growth on exclusive oral feeding after 6–12 months of gastrostomy supplemental feeding.
Discussion As the importance of nutrition in CF management became increasingly evident, efforts were made within the RCH CF service to increase formal Gastroenterology and Dietetics involvement in the clinic. One of the first tasks of the appointed gastroenterologist was to conduct an audit of gastrostomy feeding within the service to assess utilisation of this important intervention. The results of this audit found that significant malnutrition (as indicated by a WAZ score more than 2 standard deviations below the population mean) and advanced lung disease (predicted FEV1 of less than 50%) at the time of gastrostomy placement were significantly associated with a poor clinical outcome.18 As a result of this audit and a review of CF services in 2001, several initiatives were put in place, including an expansion of the dietetics service (increase from one to two staff dietitians) for children with CF. The aim was to identify at-risk children earlier and to educate parents that a gastrostomy was not a ‘pre-terminal’ event. In addition, the frequency of review appointments was increased from 4 to 6 per year. This
Table 2 Data analysis of each time point 2 year pre WAZ HAZ FEV1 (%)
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1989–1997 2002–2010 1989–1997 2002–2010 1989–1997 2002–2010
−1.82 [±0.79] −0.85 [±0.69] −1.09 [±0.83] −0.7 [±0.7] 56.9 [±16.2] 81.8 [±21.3]
1 year pre −1.9 [±0.95] −1.25 [±0.7] −1.12 [±1.0] −0.96 [±0.65] 57.3 [±16.6] 70.1 [±22.6]
PEG insertion
1 year post
2 yr post
−2.67 [±1.06] −1.5 [±0.72] −1.41 [±1.02] −1.1 [±0.77] 52.4 [±18.5] 67.7 [±23.2]
−2.44 [±1.15] −1.24 [±0.6] −1.43 [±1.03] −1.23 [±0.73] 43 [±22.2] 66.5 [±17.7]
−2.48 [±1.56] −1.2 [±0.59] −1.43 [±1.19] −1.1 [±0.5] 52.7 [±25.1] 72.7 [±17.3]
Journal of Paediatrics and Child Health 51 (2015) 988–993 © 2015 The Authors Journal of Paediatrics and Child Health © 2015 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
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Fig. 1
Fig. 2
Weight for age z-score.
Height-for-age z-score.
allowed closer observation with regard to nutritional status and facilitated a more timely and aggressive nutritional intervention. Overall, our findings are similar to several recently published prospective and retrospective studies from other CF centres. There are two studies from Queensland, Australia, in 1992 and 2009 where patients had a gastrostomy placed at a WAZ of −1.6 ± 0.4 and −1.2 ± 0.82, respectively, with a similar trend to improvement in WAZ over 2 years and stabilisation or even improvement in lung function.13,14 A cohort study of 46 patients with CF (adults and children) from Minnesota, USA, also demonstrated similar outcomes in lung function and BMI.15 Walker17 demonstrated an improvement in WAZ from −2 ± 0.87 at insertion to −1.14 ± 0.87, n = 16 with a plateauing of lung function. In addition to these findings, our re-audit demonstrated that a review of services and subsequent optimisation based on audit data led to an adaptation of the clinical care model in CF patients and improved clinical outcomes. We found no significant differences between the two cohorts with respect to age at gastrostomy insertion, gender or CF genetics. However, there were substantial differences in the timing of gastrostomy insertion with respect to the anthropometric and lung function parameters. Anthropometric data (Table 1) dem-
Gastrostomy feeding in paediatric CF
Fig. 3
Forced expiratory 1-second volume (FEV1).
onstrates that gastrostomy feeding was commenced at higher WAZ scores (P = 0.0001) in the current cohort. Lung function (FEV1) was also substantially better at that the time of insertion (P = 0.006). The WAZ for the 2002–2010 cohort improved significantly and was maintained at 2 years post-gastrostomy placement. This substantial improvement was not seen in the 1989–1997 group. Lung function was significantly different at every time point and, although both groups showed a pattern of stabilisation, this was not statistically significant. It can be noted that even in the earlier cohort there was a plateauing of lung function. These data suggest that by the time of the second audit, nutritional care in our patients had at least in part contributed to higher WAZ, as well as improved FEV1. There were significant differences in mortality between the two groups (70% vs. 100%), which cannot be attributed to the earlier nutritional intervention alone. There were multiple confounding factors that may have resulted in a better outcome of the more recent cohort. Significant confounders include improved pulmonary care and a major effect of reduced P. aeruginosa colonisation rates (100% vs. 41%). Studies such as the German Cystic Fibrosis Quality Assurance project demonstrated that malnourished patients of all ages and those with P. aeruginosa infection had significantly worse lung function and a greater yearly loss of FEV1% predicted compared with their normally nourished counterparts.22 This observation would suggest that the presence of P. aeruginosa alone would have contributed heavily to towards poorer outcomes in our earlier cohort. The sample size in this study is small, and this would limit drawing strong conclusions based on our results. Our study was a follow-up analysis within the RCH CF clinic, and so was, by definition, limited to this small group of patients. However, because the aim was to demonstrate an improvement in referral practices and nutritional support in this clinic, the numbers should suffice.
Conclusion This paper presents the completion of an audit loop looking at the quality of care provided to our patients with CF. As a result of increasing the resources with respect to dietetics and adding
Journal of Paediatrics and Child Health 51 (2015) 988–993 © 2015 The Authors Journal of Paediatrics and Child Health © 2015 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
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increased outpatient follow-up, we were able to identify at risk patients and intervene in a much more timely manner. Due to the improvements in CF management across the spectrum, ranging from better respiratory care, inhaled hypertonic saline, azithromycin use, cohorting of patients by colonisation status and other newer generation therapies, it is clear that the observed improvements were not solely due to better nutritional care. However, we speculate that aggressive nutritional management plays an important role in achieving optimum clinical outcomes in terms of nutritional status, pulmonary function and long-term survival.
Questions: 1. Gastrostomy insertion in patients with CF: a. Should be recommended in all patients losing weight b. Is reserved for the most severe patients with poor lung function c. Should be recommended in all patients with weight loss greater than 2 centile bands or who failed to reach BMI between 10–25th centile d. Should be recommended on consensus of treating gastroenterologist, respiratory physician and nutritionist if weight parameters do not improve after 3- to 6-month intensive nutritional counselling and oral nutritional support e. Is only of benefit in patients who do not successfully consume recommended dietary intake for age and weight 2. Causes of inadequate weight gain in CF include: a. Poor oral intake b. Inappropriate or inadequate use of pancreatic enzyme replacement (PERT) c. Recurrent or chronic respiratory infection d. Associated conditions such as diabetes mellitus, celiac disease etc, or psychosocial issues e. All of the above 3. The main aim of quality audits in clinical practice is to: a. Identify areas of underperformance b. Compare outcomes with other centres c. Lead to improvement in patient outcomes d. Appropriately lay the blame on the poorly performing party e. Facilitate accreditation
Answers: 1. D a. Weight loss can usually be addressed successfully with other measures including rationalising pancreatic enzyme replacement, supplemental oral nutrition and addressing other medical and psychosocial concerns b. Gastrostomy insertion should be recommended before patients deteriorate significantly in order to prevent deterioration. c. While this is significant weight loss, other interventions with close follow-up should be considered prior to recommending gastrostomy d. Gastrostomy should be used early when other interventions have failed to address malnutrition 992
e. Recommended dietary intake may be inadequate in some CF patients due to other causes of increased energy expenditure or energy malabsorption in CF 2. E a. Anorexia may be due to recurrent or chronic infection, symptomatic gastro-oesophageal reflux disease b. Dose of PERT may be insufficient, or may be improved with gastric acid suppression c. Recurrent or chronic infection can impair weight gain due to energy expenditure of inflammation and anorexia related to inflammatory cytokines d. Other medical and psychosocial issues, both related and unrelated to CF may further impair weight gain e. There are many factors which can impair weight gain, and all these must be thoroughly investigated in managing these children 3. C a. This is correct, but is not an end-point in itself b. Comparing outcomes is important to try set a benchmark; however, this is not the ultimate goal of quality audits c. This must be the constant focus of all quality interventions in clinical practice d. Quality improvement measures should never be performed in a negative approach aiming to seek blame e. Accreditation is important, but this serves as a means to an end.
References 1 Corey M, McLaughlin FJ, Williams M, Levison H. A comparison of survival, growth and pulmonary function in patients with cystic fibrosis in Boston and Toronto. J. Clin. Epidemiol. 1988; 41: 583–91. 2 Milla CE. Association of nutritional status and pulmonary function in children with cystic fibrosis. Curr. Opin. Pulm. Med. 2004; 10: 505–9. 3 Bradley GM, Carson KA, Leonard AR, Mogayzel PJ Jr, Oliva-Hemker M. Nutritional outcomes following gastrostomy in children with cystic fibrosis. Pediatr. Pulmonol. 2012; 47: 743–8. 4 Akobeng AK, Miller V, Thomas A. Percutaneous endoscopic gastrostomy feeding improves nutritional status and stabilizes pulmonary function in patients with cystic fibrosis. J. Pediatr. Gastroenterol. Nutr. 1999; 29: 485–6. 5 Zemel BS, Kawchak DA, Cnaan A, Zhao H, Scanlin TF, Stallings VA. Prospective evaluation of resting energy expenditure, nutritional status, pulmonary function, and genotype in children with cystic fibrosis. Pediatr. Res. 1996; 40: 578–86. 6 Pencharz PB, Durie PR. Pathogenesis of malnutrition in cystic fibrosis, and its treatment. Clin. Nutr. 2000; 19: 387–94. 7 Holt TL, Ward LC, Francis PJ, Isles A, Cooksley WG, Shepherd RW. Whole body protein turnover in malnourished cystic fibrosis patients and its relationship to pulmonary disease. Am. J. Clin. Nutr. 1985; 41: 1061–6. 8 Anthony H, Paxton S, Catto-Smith A, Phelan P. Physiological and psychosocial contributors to malnutrition in children with cystic fibrosis: review. Clin. Nutr. 1999; 18: 327–35. 9 Roulet M. Protein-energy malnutrition in cystic fibrosis patients. Acta Paediatr. Suppl. 1994; 83: 43–8. 10 Durie PR, Pencharz PB. Cystic fibrosis: nutrition. Br. Med. Bull. 1992; 48: 823–46. 11 Borowitz D, Baker RD, Stallings V. Consensus report on nutrition for pediatric patients with cystic fibrosis. J. Pediatr. Gastroenterol. Nutr. 2002; 35: 246–59.
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12 Steinkamp G, von der Hardt H. Improvement of nutritional status and lung function after long-term nocturnal gastrostomy feedings in cystic fibrosis. J. Pediatr. 1994; 124: 244–9. 13 Truby H, Cowlishaw P, O’Neil C, Wainwright C. The longterm efficacy of gastrostomy feeding in children with cystic fibrosis on anthropometric markers of nutritional status and pulmonary function. Open Respir. Med. J. 2009; 3: 112–15. 14 Dalzell AM, Shepherd RW, Dean B, Cleghorn GJ, Holt TL, Francis PJ. Nutritional rehabilitation in cystic fibrosis: a 5 year follow-up study. J. Pediatr. Gastroenterol. Nutr. 1992; 15: 141–5. 15 Best C, Brearley A, Gaillard P et al. A pre-post retrospective study of patients with cystic fibrosis and gastrostomy tube. J. Pediatr. Gastroenterol. Nutr. 2011; 53: 453–8. 16 Efrati O, Mei-Zahav M, Rivlin J et al. Long term nutritional rehabilitation by gastrostomy in Israeli patients with cystic fibrosis: clinical outcome in advanced pulmonary disease. J. Pediatr. Gastroenterol. Nutr. 2006; 42: 222–8. 17 Walker SA, Gozal D. Pulmonary function correlates in the prediction of long-term weight gain in cystic fibrosis patients with gastrostomy tube feeding. J. Pediatr. Gastroenterol. Nutr. 1998; 27: 53–6.
18 Oliver MR, Heine RG, Ng CH, Volders E, Olinsky A. Factors affecting clinical outcome in gastrostomy-fed children with cystic fibrosis. Pediatr. Pulmonol. 2004; 37: 324–9. 19 Anthony H, Collins CE, Davidson G et al. Pancreatic enzyme replacement therapy in cystic fibrosis: Australian guidelines. Pediatric Gastroenterological Society and the Dietitians Association of Australia. J. Paediatr. Child Health 1999; 35: 125–9. 20 Dibley MJ, Goldsby JB, Staehling NW, Trowbridge FL. Development of normalized curves for the international growth reference: historical and technical considerations. Am. J. Clin. Nutr. 1987; 46: 736–48. 21 Crapo RO, Morris AH, Gardner RM. Reference spirometric values using techniques and equipment that meet ATS recommendations. Am. Rev. Respir. Dis. 1981; 123: 659–64. 22 Steinkamp G, Wiedemann B. Relationship between nutritional status and lung function in cystic fibrosis: cross sectional and longitudinal analyses from the German CF quality assurance (CFQA) project. Thorax 2002; 57: 596–601.
Sydney by Lucy Beford (11) from Operation Art 2014.
Journal of Paediatrics and Child Health 51 (2015) 988–993 © 2015 The Authors Journal of Paediatrics and Child Health © 2015 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
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doi:10.1111/jpc.12888
ORIGINAL ARTICLE
Clinical audit results in earlier nutritional intervention in malnourished children with cystic fibrosis with improved outcome Oren Ledder,1 Mark R Oliver,1,2,3 Ralf G Heine,1,2,3 Joanne Graham,4 Evelyn Volders5 and Philip J Robinson2,3,4 Departments of 1Gastroenterology and Clinical Nutrition and 4Respiratory Medicine, Royal Children’s Hospital, 2Department of Paediatrics, University of Melbourne, 3Murdoch Childrens Research Institute, and 5Department of Nutrition & Dietetics, Monash University, Melbourne, Victoria, Australia
Aim: The association between nutritional status, pulmonary function and survival in cystic fibrosis (CF) is well established. A previous case series from the Royal Children’s Hospital, Melbourne (RCH), demonstrated suboptimal referral practices and highlighted the importance of early nutritional interventions in children with CF. Various qualitative changes were made to our CF service, and this study assesses the effects of these practice changes timing of gastrostomy and clinical outcome in patients who underwent gastrostomy insertion. Method: Clinical audit of all CF patients who had undergone gastrostomy insertion from 2002 to 2010 at Royal Children’s Hospital. Clinical data, including nutritional parameters, respiratory function and survival, were collected at 2 years prior and 2 years post gastrostomy insertion. Data were compared with the previous study from 1989 to 1997. Results: Patients with CF who underwent gastrostomy insertion between 2002 and 2010 (n = 22) had higher weight-for-age scores (−1.5 ± 0.68 vs. −2.67 ± 1.06; P = 0.0001) and higher forced expiratory volume in 1 s (68% ± 22 vs. 52% ± 18.5; P = 0.006), compared with the cohort from 1989 to 1997 (n = 37). These differences were maintained at 2-year follow-up. Pseudomonas aeruginosa colonisation rate was 100% in 1989–1997 vs. 41% in 2002–2010; P = 0.0001. The 2-year survival post-gastrostomy insertion improved from 70% to 100%; P = 0.004. Conclusion: Earlier referral of patients in the recent cohort resulted in sustained improvements in weight-for-age and lung function. Survival at 2 years post-procedure was significantly improved. This study confirms the value of clinical audits and subsequent re-evaluation of clinical services. Key words:
gastroenterology; nutrition, respiratory.
What is already known on this topic
What this paper adds
1 Aggressive nutritional support is associated with improved outcomes in malnourished patients with cystic fibrosis (CF) and has been shown to improve lung function, as well as overall survival. 2 A structured, multidisciplinary CF clinic leads to improved patient care and better outcomes. 3 Quality audits are a critical component in continuously improving clinical service.
1 Close involvement of nutrition and gastroenterological services in a multidisciplinary CF clinic aids in the early detection of malnutrition in CF patients and facilitates insertion of gastrostomy at a more timely stage. 2 More timely insertion of a gastrostomy in malnourished CF patients contributes positively to better growth, lung function and possibly survival. 3 Quality audit directed implementation of clinical practice changes should be re-evaluated with repeat audits to verify outcomes (closing the audit-loop).
The close association between nutritional status, pulmonary function and survival in cystic fibrosis (CF) is generally accepted.1–4 Children and adolescents with advanced CF are often unable to meet their rapidly increasing energy requirements.5 Anorexia associated with chronic lung infection, nutrient maldigestion and malabsorption, gastro-oesophageal reflux Correspondence: Dr Mark R Oliver, Department of Gastroenterology and Clinical Nutrition, Royal Children’s Hospital, Flemington Road, Parkville, Vic. 3052, Australia. Fax: +61·39345 6240; email: [email protected] Conflict of interest: None. Accepted for publication 2 March 2015.
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disease and glucosuria, among others, are important factors leading to the development of malnutrition.6 Furthermore, a high total body muscle turnover predisposes patients with CF to respiratory muscle wasting which, in turn, may accelerate the progression of lung disease.7 Successful nutritional programmes have recognised the need to address not only these physiological factors, but also the psychosocial circumstances contributing to malnutrition.8 Such programmes have reduced the prevalence of nutritional deficiency states and protein-energy malnutrition.9 Some malnourished patients fail to respond to intensive multidisciplinary support such as education, dietary advice, optimisation of pancreatic replacement therapy and intensive
Journal of Paediatrics and Child Health 51 (2015) 988–993 © 2015 The Authors Journal of Paediatrics and Child Health © 2015 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
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treatment of pulmonary exacerbations.10 For these patients, the US CF Foundation recommends early intervention with aggressive nutritional supplementation via nasogastric or gastrostomy feeding.11 Long-term nutritional rehabilitation by gastrostomy has been shown to significantly improve weight, height and body mass index (BMI) z-scores and may ameliorate the progression of the pulmonary disease.12–17 Clinical care is provided for over 300 children with CF at the Royal Children’s Hospital in Melbourne (RCH). A previous study at RCH in children with CF demonstrated suboptimal referral practices and supported the importance of early nutritional intervention, such as supplemental feeds, pancreatic enzyme replacement optimisation and referral for gastrostomy insertion.18 As a result of this review, an additional full-time dietitian was appointed in 2002, and second-monthly rather than third-monthly outpatient visits were instituted in an attempt to facilitate a more aggressive approach to nutritional care of the patients. A further change included improved cohorting of patients according their pulmonary colonisation status. This retrospective study was primarily aimed at assessing whether improved dietetic and clinical follow-up impacted on the referral pattern of our patients from the pulmonologists (who provide the majority of the primary care of these patients) to the gastroenterology service. We also aimed to see if this led to better clinical outcomes in terms of weight gain and lung function. We therefore conducted a second clinical audit, comparing our current CF cohort to our previously published cohort of 37 patients with CF.18
Methods We conducted a retrospective clinical audit of all patients with CF at RCH who required gastrostomy insertion for nutritional management between 2002 and 2010. This clinical audit was approved by the Ethics in Human Research Committee at the Royal Children’s Hospital, Melbourne. We retrieved data for patients with CF who received gastrostomy feeds between 1989 and 1997, whom we had previously studied, and compared these with the current cohort.18 The diagnosis of CF was confirmed in all patients on the basis of clinical manifestations and abnormal sweat chloride. All patients were pancreatic insufficient, as demonstrated by either an abnormal 3-day faecal fat balance, or the presence of fat globules on faecal microscopy, in conjunction with a clinical history of steatorrhoea. Children with persistent poor weight gain were assessed for nutritional intake, and other causes for poor weight gain, such as diabetes mellitus or coeliac disease, were excluded on clinical and laboratory grounds. Adherence to pancreatic enzyme therapy was closely monitored during this period. Proton pump inhibitors were prescribed for a period of 3–6 months as an adjunct therapy to aid fat absorption, as per Australian CF guidelines on pancreatic enzyme replacement therapy.19 Prior to gastrostomy insertion, patients were closely monitored by our multidisciplinary team that included a pulmonologist, gastroenterologist, dietitian and clinical psychologist. Patients were provided with printed information regarding gastrostomy and enteral feeds. Gastrostomy insertion was recommended in the current group by consensus of the treating pulmonologist, gastroenterologist and dietitian if weight loss was greater than 2 bands on the
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growth chart or if there was lack of improvement in children to reach the target BMI 10–25th percentile after a 3- to 6-month period of intensive dietary counselling and oral energy supplementation.17 After gastrostomy insertion, patients were asked to use their gastrostomy tube for supplemental feeding on five to six nights per week. Patients were prescribed dietary supplements providing 30–40 kcal/kg (125–170 kJ/kg) per day, which were administered by continuous overnight infusion. Pancreatic enzymes were administered at the commencement and completion of gastrostomy feeds. This feeding protocol utilised a standard nutritionally balanced polymeric formula with scope for different manufacturers and brands as per preference or availability. Ongoing assessment of compliance was assessed during regular 2nd–3rd monthly clinic reviews with both the treating physician and the dietician. All costs of nutritional supplementation were covered by a state government programme, effectively neutralising the cost burden of supplemental formula to assist compliance regardless of socio-economic circumstances. Weight, height and respiratory function tests were measured during the period 2 years before and after gastrostomy insertion in both cohorts. The best achieved spirometry measurements at each time point was recorded and used for the data comparisons between the two cohorts. Colonisation rates with Pseudomonas aeruginosa and 2-year survival were also recorded. Data for the 1989–1997 cohort was re-analysed using the current statistical methods (rather than weighted means that we used in the previously analysis). Standard deviation scores (z-scores) for weight-for-age (WAZ) and height-for-age (HAZ) were calculated using the epidemiological software program Epi Info 2000 (Centers for Disease Control and Prevention, Atlanta, GA, USA).20 Spirometry measurements were obtained from all patients 5 years and older, and the forced expiratory volume in 1 second (FEV1) was expressed as percentage predicted, after adjusting for weight, height and gender.21 Comparisons of growth and lung function data were made between the cohorts of 2002–2010 and 1989–1997. The study was divided into five time points (i.e. 2 years before, 1 year before, at time of insertion, 1 year post-gastrostomy insertion and 2 years postgastrostomy insertion).
Data analysis Normally distributed data were presented as mean ± standard deviation, or as median and interquartile range for skewed data. Anthropometric and lung function data at a time point in both cohorts were compared with each other using the unpaired two-sample t-test. To assess changes in lung function and anthropometric data within each cohort over time, a repeated measure analysis of variance was used. Fisher’s exact test was used to assess rates of survival and colonisation with P. aeruginosa. All data analyses were performed using GraphPad Prism 5 software (GraphPad Software, Inc. La Jolla, CA, USA).
Results Characteristics of the 2002–2010 cohort Between 2002 and 2010, 22 patients (mean age 9.7 ± 2.7 years; 12 female (54.5%) ) with CF underwent gastrostomy insertion
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in order to improve their nutritional status. All children were pancreatic insufficient. Fifty-eight per cent of children were homozygous, and 33% were heterozygous for ΔF508 deletion. One child was below the age of 5 years at the time of gastrostomy insertion and was unable to perform lung function tests. Nine patients were colonised with P. aeruginosa and two had CF-related diabetes mellitus at the time of insertion. No patient died during the 2-year follow-up period.
Characteristics of the 1989–1997 cohort There were 37 patients (mean age 11.6 ± 4.8 years, 15 female (40.5%) ). All were pancreatic insufficient and colonised with P. aeruginosa. Fifty-six per cent of children were homozygous and 22% were heterozygous for ΔF508 deletion. Eleven patients (seven female (64.6%)) died during the 2-year follow-up, with a median survival of 0.91 years (interquartile range 0.18–1.26).
Comparison of data for cohort from 1989–1997 and 2002–2010 The mean age at the time of gastrostomy insertion was similar for both cohorts (11.6 years ± 4.8 vs. 9.7 years ± 2.7; P = 0.14). The cohort of 1989–1997 had significantly lower WAZ scores at gastrostomy insertion (WAZ −2.67 ± 1.06 vs. −1.53 ± 0.68; P = 0.0001). Lung function was also significantly lower for the earlier cohort (FEV1 52% ± 18.5 vs. 68% ± 22; P = 0.006). There were no substantial differences in HAZ scores between cohorts. Gastrostomy insertion occurred at a substantially higher BMI centile in the recent cohort, compared with the original group
Table 1 Comparison of patient characteristics at the time of gastrostomy insertion between both cohorts
Number of patients Mean age (SD) at insertion Gender (M:F) WAZ score HAZ score FEV1 (% predicted) P. aeruginosa positive (n (%) ) Survival 2 years post PEG (n (%) )
1989–1997
2002–2010
P value
37 11.6 (±4.8) 1.47 : 1 −2.67 (±1.06) −1.41 (±1.02) 52 (±18) 37 (100) 26 (70)
22 9.7 (±2.7) 0.83 : 1 −1.53 (±0.68) −1.06 (±0.76) 68 (±22) 9 (41) 100%
0.14 0.42 0.0001 0.17 0.006 0.0001 0.004
(19.5 ± 16.2 vs. 3.4 ± 6.9; P = 0.0001). There was a dramatic reduction in pulmonary colonisation rates with P. aeruginosa from 100% in the previous cohort to 41% in the current group (P = 0.0001). The 2-year survival was 70% in the earlier cohort and 100% in the recent cohort (P = 0.004) (Table 1). Anthropometric and lung function data for both cohorts were compared between the time of insertion and four other time points: −2, −1, +1 and +2 years (Table 2). For weight (WAZ), there were significant differences at all four time points (Fig. 1). For the 2002–2010 cohort, WAZ improved from −1.53 ± 0.68 at insertion to −1.0 ± 0.68 at +2 years; P = 0.01. For the 1989–1997 cohort, the increase in WAZ was not significant (WAZ −2.67 ± 1.06 at insertion vs. −2.48 ± 1.55 at +2 years; N.S.). With respect to height (HAZ), data are summarised in Figure 2. There were no significant differences at any time point between the two cohorts. For FEV1, there were significant differences at all the time points (Fig. 3). Mean FEV1 in the 2002–2010 cohort fell from 81.8% ± 21 (n = 19) at –2 years to 68% ± 22 (n = 21) at insertion (P = 0.07) and remained stable at +2 years (68% ± 19 (n = 22) ). For the 1989–1997 cohort, a similar pattern was observed (Fig. 3). Of note, one child in each cohort had their gastrostomy removed after demonstrating persistent successful weight gain and growth on exclusive oral feeding after 6–12 months of gastrostomy supplemental feeding.
Discussion As the importance of nutrition in CF management became increasingly evident, efforts were made within the RCH CF service to increase formal Gastroenterology and Dietetics involvement in the clinic. One of the first tasks of the appointed gastroenterologist was to conduct an audit of gastrostomy feeding within the service to assess utilisation of this important intervention. The results of this audit found that significant malnutrition (as indicated by a WAZ score more than 2 standard deviations below the population mean) and advanced lung disease (predicted FEV1 of less than 50%) at the time of gastrostomy placement were significantly associated with a poor clinical outcome.18 As a result of this audit and a review of CF services in 2001, several initiatives were put in place, including an expansion of the dietetics service (increase from one to two staff dietitians) for children with CF. The aim was to identify at-risk children earlier and to educate parents that a gastrostomy was not a ‘pre-terminal’ event. In addition, the frequency of review appointments was increased from 4 to 6 per year. This
Table 2 Data analysis of each time point 2 year pre WAZ HAZ FEV1 (%)
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1989–1997 2002–2010 1989–1997 2002–2010 1989–1997 2002–2010
−1.82 [±0.79] −0.85 [±0.69] −1.09 [±0.83] −0.7 [±0.7] 56.9 [±16.2] 81.8 [±21.3]
1 year pre −1.9 [±0.95] −1.25 [±0.7] −1.12 [±1.0] −0.96 [±0.65] 57.3 [±16.6] 70.1 [±22.6]
PEG insertion
1 year post
2 yr post
−2.67 [±1.06] −1.5 [±0.72] −1.41 [±1.02] −1.1 [±0.77] 52.4 [±18.5] 67.7 [±23.2]
−2.44 [±1.15] −1.24 [±0.6] −1.43 [±1.03] −1.23 [±0.73] 43 [±22.2] 66.5 [±17.7]
−2.48 [±1.56] −1.2 [±0.59] −1.43 [±1.19] −1.1 [±0.5] 52.7 [±25.1] 72.7 [±17.3]
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Fig. 1
Fig. 2
Weight for age z-score.
Height-for-age z-score.
allowed closer observation with regard to nutritional status and facilitated a more timely and aggressive nutritional intervention. Overall, our findings are similar to several recently published prospective and retrospective studies from other CF centres. There are two studies from Queensland, Australia, in 1992 and 2009 where patients had a gastrostomy placed at a WAZ of −1.6 ± 0.4 and −1.2 ± 0.82, respectively, with a similar trend to improvement in WAZ over 2 years and stabilisation or even improvement in lung function.13,14 A cohort study of 46 patients with CF (adults and children) from Minnesota, USA, also demonstrated similar outcomes in lung function and BMI.15 Walker17 demonstrated an improvement in WAZ from −2 ± 0.87 at insertion to −1.14 ± 0.87, n = 16 with a plateauing of lung function. In addition to these findings, our re-audit demonstrated that a review of services and subsequent optimisation based on audit data led to an adaptation of the clinical care model in CF patients and improved clinical outcomes. We found no significant differences between the two cohorts with respect to age at gastrostomy insertion, gender or CF genetics. However, there were substantial differences in the timing of gastrostomy insertion with respect to the anthropometric and lung function parameters. Anthropometric data (Table 1) dem-
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Fig. 3
Forced expiratory 1-second volume (FEV1).
onstrates that gastrostomy feeding was commenced at higher WAZ scores (P = 0.0001) in the current cohort. Lung function (FEV1) was also substantially better at that the time of insertion (P = 0.006). The WAZ for the 2002–2010 cohort improved significantly and was maintained at 2 years post-gastrostomy placement. This substantial improvement was not seen in the 1989–1997 group. Lung function was significantly different at every time point and, although both groups showed a pattern of stabilisation, this was not statistically significant. It can be noted that even in the earlier cohort there was a plateauing of lung function. These data suggest that by the time of the second audit, nutritional care in our patients had at least in part contributed to higher WAZ, as well as improved FEV1. There were significant differences in mortality between the two groups (70% vs. 100%), which cannot be attributed to the earlier nutritional intervention alone. There were multiple confounding factors that may have resulted in a better outcome of the more recent cohort. Significant confounders include improved pulmonary care and a major effect of reduced P. aeruginosa colonisation rates (100% vs. 41%). Studies such as the German Cystic Fibrosis Quality Assurance project demonstrated that malnourished patients of all ages and those with P. aeruginosa infection had significantly worse lung function and a greater yearly loss of FEV1% predicted compared with their normally nourished counterparts.22 This observation would suggest that the presence of P. aeruginosa alone would have contributed heavily to towards poorer outcomes in our earlier cohort. The sample size in this study is small, and this would limit drawing strong conclusions based on our results. Our study was a follow-up analysis within the RCH CF clinic, and so was, by definition, limited to this small group of patients. However, because the aim was to demonstrate an improvement in referral practices and nutritional support in this clinic, the numbers should suffice.
Conclusion This paper presents the completion of an audit loop looking at the quality of care provided to our patients with CF. As a result of increasing the resources with respect to dietetics and adding
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increased outpatient follow-up, we were able to identify at risk patients and intervene in a much more timely manner. Due to the improvements in CF management across the spectrum, ranging from better respiratory care, inhaled hypertonic saline, azithromycin use, cohorting of patients by colonisation status and other newer generation therapies, it is clear that the observed improvements were not solely due to better nutritional care. However, we speculate that aggressive nutritional management plays an important role in achieving optimum clinical outcomes in terms of nutritional status, pulmonary function and long-term survival.
Questions: 1. Gastrostomy insertion in patients with CF: a. Should be recommended in all patients losing weight b. Is reserved for the most severe patients with poor lung function c. Should be recommended in all patients with weight loss greater than 2 centile bands or who failed to reach BMI between 10–25th centile d. Should be recommended on consensus of treating gastroenterologist, respiratory physician and nutritionist if weight parameters do not improve after 3- to 6-month intensive nutritional counselling and oral nutritional support e. Is only of benefit in patients who do not successfully consume recommended dietary intake for age and weight 2. Causes of inadequate weight gain in CF include: a. Poor oral intake b. Inappropriate or inadequate use of pancreatic enzyme replacement (PERT) c. Recurrent or chronic respiratory infection d. Associated conditions such as diabetes mellitus, celiac disease etc, or psychosocial issues e. All of the above 3. The main aim of quality audits in clinical practice is to: a. Identify areas of underperformance b. Compare outcomes with other centres c. Lead to improvement in patient outcomes d. Appropriately lay the blame on the poorly performing party e. Facilitate accreditation
Answers: 1. D a. Weight loss can usually be addressed successfully with other measures including rationalising pancreatic enzyme replacement, supplemental oral nutrition and addressing other medical and psychosocial concerns b. Gastrostomy insertion should be recommended before patients deteriorate significantly in order to prevent deterioration. c. While this is significant weight loss, other interventions with close follow-up should be considered prior to recommending gastrostomy d. Gastrostomy should be used early when other interventions have failed to address malnutrition 992
e. Recommended dietary intake may be inadequate in some CF patients due to other causes of increased energy expenditure or energy malabsorption in CF 2. E a. Anorexia may be due to recurrent or chronic infection, symptomatic gastro-oesophageal reflux disease b. Dose of PERT may be insufficient, or may be improved with gastric acid suppression c. Recurrent or chronic infection can impair weight gain due to energy expenditure of inflammation and anorexia related to inflammatory cytokines d. Other medical and psychosocial issues, both related and unrelated to CF may further impair weight gain e. There are many factors which can impair weight gain, and all these must be thoroughly investigated in managing these children 3. C a. This is correct, but is not an end-point in itself b. Comparing outcomes is important to try set a benchmark; however, this is not the ultimate goal of quality audits c. This must be the constant focus of all quality interventions in clinical practice d. Quality improvement measures should never be performed in a negative approach aiming to seek blame e. Accreditation is important, but this serves as a means to an end.
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Sydney by Lucy Beford (11) from Operation Art 2014.
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