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BRONCHIOLITIS: KEEP IT SIMPLE, A BEFORE AND AFTER

FRENCH STUDY

Journal: BMJ Paediatrics Open

Manuscript ID bmjpo-2017-000089

Article Type: Original article

Date Submitted by the Author: 21-May-2017

Complete List of Authors: Benhamida, Myriam; Centre Hospitalier Universitaire de Nantes, BIHOUEE, Tiphaine; Centre Hospitalier Universitaire de Nantes Verstraete, Marie; Centre Hospitalier Universitaire de Nantes Gras Le Guen, Christèle; Centre Hospitalier Universitaire de Nantes Launay, Elise; Centre Hospitalier Universitaire de Nantes

Keywords: Evidence Based Medicine, General Paediatrics, Infectious Diseases, Respiratory

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TITLE PAGE 1

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TITLE: 3

BRONCHIOLITIS: KEEP IT SIMPLE, A BEFORE AND AFTER FRENCH STUDY 4

5

AUTHORS: 6

Myriam BENHAMIDA M.¹, E-mail [email protected] 7

Tiphaine BIHOUEE ¹, E-mail: [email protected] 8

Marie VERSTRAETE ¹, E-mail: [email protected] 9

Christèle GRAS LE GUEN.¹, E-mail: [email protected] 10

Elise LAUNAY ¹, E-mail: [email protected] 11

12

AUTHOR AFFILIATIONS 13

¹Clinique Médicale de Pédiatrie, Hôpital Mère Enfant, Centre Hospitalier Universitaire 14

Nantes, , 7 quai Moncousu 44093, Nantes Cedex 1, France 15

16

CORRESPONDENCE TO: Myriam Benhamida 17

Adress : Clinique Médicale de Pédiatrie, CHU de Nantes, 7 quai Moncousu 44093, Nantes 18

Cedex 1, France 19

Phone : +33 2.40.08.44.54 20

E-mail: [email protected] 21

The results of this study were presented at the annual meeting of the French Pediatric 22

Society in May 2016 in Lille (France) 23

24

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ABSTRACT 25

(i) The most recent French bronchiolitis guidelines were published in 2000. In 2012, the 26

Group of Pediatric University Hospitals in Western France (‘HUGO’) proposed new evidence-27

based clinical practice guidelines. In keeping with the latest international guidelines, they 28

recommend reducing unnecessary treatments and diagnostic tests. The aim study was to 29

determine the impact of these guidelines on the management of bronchiolitis inpatients. 30

(ii) This retrospective before after design study was conducted in the general pediatric unit of 31

a tertiary level of care French hospital, either one year before (i.e. the winter of 2011-2012) 32

or one year after (i.e. the winter of 2013-2014) implementation of the guidelines. 280 33

bronchiolitis inpatients, less than one year of age, were included. The primary outcome was 34

the proportion of children administered a diagnostic test associated with a treatment not 35

routinely recommended by the guidelines. As balancing measures we evaluated the length of 36

stay, the ICU transfer and the readmission rates. 37

(iii) Following implementation of the guidelines, use of any given treatment associated with a 38

diagnostic test was reduced by 66% (p<0.001). There were major decreases in the use of 39

chest-X-ray (86% vs 26%, p<0.001), antibiotics (38.23% vs 13.33%, p<0.001), and 40

corticosteroids (10.43% vs 3.03%, p=0.011). Balancing measures were not significantly 41

different. 42

(iv) HUGO guidelines were effective at reducing the administration of unnecessary diagnostic 43

tests and medications on a French population, without causing a discernible adverse effect. 44

Further research is needed to assess if these changes are sustained over time, and can be 45

broadened at other hospitals. 46

47

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KEYWORDS: bronchiolitis, guidelines, resource utilization 48

49

WHAT IS KNOWN? 50

• The latest international bronchiolitis guidelines recommend reducing unnecessary 51

treatments and diagnostic tests. 52

• Many North American studies have revealed reductions in resource utilization and 53

costs following the implementation of these guidelines. 54

• There is currently a substantial variability in bronchiolitis inpatient management 55

throughout hospitals in Europe. 56

WHAT IS NEW? 57

• This work is the first French study assessing the impact of a recent set of bronchiolitis 58

inpatient management guidelines. 59

• Reducing the administration of unnecessary diagnostic tests and medications on a 60

French population is possible, without causing a discernible adverse effect. 61

62

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ABREVIATIONS 63

AAP American Academy of Pediatrics

CRP C-reactive protein

CPS Canadian Pediatric Society

CXR Chest X-ray

ESPID European Society for Paediatric Infectious Diseases

FBC Full blood count

GP General pediatric

HUGO Group of Pediatric University Hospitals in Western France

ICU Intensive care unit

IQR Interquartile range

LOS Length of stay

NICE National Institute for Health and Care Excellence

NUH Nantes University Hospital

PCT Procalcitonin

PMSI Medical Program of Information Systems

RSV Respiratory syncytial virus

64

65

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TEXT 66

INTRODUCTION 67

Acute viral bronchiolitis results in 30,000 hospitalizations annually in France [1]. The most 68

recent French guidelines date from 2000 [2], while other pediatric national societies such as 69

the National Institute for Health and Care Excellence (NICE) [3], the American Academy of 70

Pediatrics (AAP) [4], and the Canadian Pediatric Society (CPS) have provided new evidence-71

based clinical practice guidelines for the management of bronchiolitis inpatients [5]. They 72

recommend curtailing the excessive use of antibiotics, chest X-rays (CXR), and blood tests, 73

as well as unnecessary treatments such as the administration of corticosteroids, salbutamol, 74

and chest physiotherapy. They also specify the modalities for administering supplemental 75

oxygen and fluid replacement. Many American studies have revealed reductions in resource 76

utilization and costs following the implementation of these guidelines without a decline in 77

health-related outcomes [6–10]. Nevertheless, some European pediatricians are still 78

reluctant to streamline their practices, as shown in the last study of the European Society for 79

Paediatric Infectious Diseases (ESPID)[11]. 80

In order to improve bronchiolitis inpatient management, the Group of Pediatric 81

University Hospitals in Western France (‘HUGO’) published guidelines in 2012 that are in 82

keeping with the latest international recommendations [12]. 83

In this study we sought to determine the impact of these HUGO guidelines. Our 84

primary aim was to evaluate whether streamlining of practices could be implemented in 85

France. We hypothesized that the proportion of patients receiving treatments such as 86

antibiotics, corticosteroids, or salbutamol, and a diagnostic test such as chest X-rays, 87

respiratory syncytial virus (RSV) testing, or a blood test would be reduced following 88

implementation of the HUGO guidelines. As secondary outcomes, we evaluated the length of 89

stay (LOS), hospitalization costs, and rates of intensive care unit (ICU) transfer and 90

readmission at seven days. We also compared the modalities of supportive care prior to and 91

following implementation of the guidelines. 92

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METHODS 93

Setting and Study Design 94

The Nantes University Hospital (NUH) provides pediatric tertiary level of care for a 95

geographical area with a population of 850,000 with 12,107 births in 2010. Every winter, 96

bronchiolitis accounts for approximately 500 hospitalizations at the NUH [13]. We conducted 97

a retrospective study of quality improvement intervention in order to standardize the care 98

provided to bronchiolitis inpatients. We compared the year prior to implementation of the 99

HUGO guidelines (i.e. the winter of 2011-2012) to the year following their implementation 100

(i.e. the winter of 2013-2014). We deemed the winter of 2012-2013 to be a transition year. 101

For each bronchiolitis season, we analyzed the three weeks of major bronchiolitis 102

epidemics. Every year, during those weeks, the NUH general pediatric unit becomes 103

overcrowded, accommodating essentially just bronchiolitis inpatients. We hypothesized that 104

the workload is similar year-over-year during those periods. According to the regional office 105

of the French Institute for Public Health of the Pays de la Loire, for the winter of 2011–2012, 106

the three major bronchiolitis epidemic weeks were weeks 48, 49, and 50. For the winter of 107

2013–2014 they were weeks 51, 52, and 1. 108

The project was approved by the institutional review board at the NUH. 109

French legislation stipulates that informed consent is not required and local retrospective 110

data may be used for an epidemiologic study. We followed SQUIRE guidelines to report this 111

study [14]. 112

Intervention: HUGO Bronchiolitis Guidelines Development and Implementation 113

In 2011, the pediatricians, pediatric pulmonologists, and emergency physicians belonging to 114

HUGO met to analyze the recent published data regarding bronchiolitis in children less than 115

one year of age. Criteria to distinguish childhood asthma from acute viral bronchiolitis were 116

established. Prescriptions of diagnostic tests, antibiotics, and chest physiotherapy were 117

defined and reserved for limited situations. Modalities of oxygen supplementation and 118

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nutritional support were proposed. All these recommendations were summarized in the 119

HUGO bronchiolitis guidelines[12]. 120

The guidelines were implemented by the NUH in September 2012, by holding team 121

meetings involving pediatric nurses, physicians, and trainees. These interprofessional 122

meetings take place every year at the start of bronchiolitis season. The guidelines were 123

integrated into the NUH guidelines book, and they are readily accessible online via the 124

hospital’s intranet website. 125

Study Population and Data Sources 126

The target population for the HUGO bronchiolitis guidelines was children from birth to one 127

year of age, who were diagnosed with bronchiolitis. The diagnosis of bronchiolitis was based 128

on their medical history and a physical examination showing viral upper respiratory tract 129

prodrome, followed by increased respiratory effort and wheezing, as recommended in the 130

HUGO and international guidelines [4,5,12,15]. 131

Using the NUH Medical Program of Information System (PMSI), we screened for all 132

patients with a bronchiolitis diagnosis defined by the group of codes “Acute Bronchiolitis” of 133

the International Classification of Disease 10 (J21, J21.0, J21.8, J21.9), and who were 134

hospitalized in the general pediatric unit of the NUH during the inclusion periods. Of these 135

patients, we excluded patients aged >12 months old, patients with a history of more than one 136

wheezing dyspnea episode, and obvious mistakes in the PMSI such as an absence of any 137

clinical signs of respiratory infection in their medical files. 138

We opted for a pragmatic study, so we did not exclude patients with comorbidities or 139

those that had required a transfer to the ICU at any time during their management. Only the 140

patient’s management in the general pediatric unit was evaluated. 141

Data were collected by the retrospective review of medical files, and tabulated using 142

Excel (Microsoft, Inc, Redmond, USA). Data on the cost of services were obtained from the 143

hospital’s administrative and financial databases for each included patient. 144

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Methods of Evaluation 145

To capture the overall impact of the HUGO guidelines, we used a composite outcome build 146

with the two main resources that tend to be misused in bronchiolitis: diagnostic tests and 147

treatments. Our primary outcome was the proportion of patients having been administered at 148

least one antibiotic, corticosteroid, or salbutamol treatment, and either a CXR, RSV testing, 149

or an inflammatory blood test. We selected these treatments and tests because their use is 150

not routinely recommended by the HUGO guidelines. Moreover, they are typical outcomes 151

used to evaluate unnecessary treatments in bronchiolitis quality improvement studies [6,8,9]. 152

As secondary outcomes, we compared total hospitalization costs (including the cost 153

of overall unit functioning, laboratory tests, imaging, drugs, supplies, and materials), the use 154

of each treatment and diagnostic test: antibiotics, salbutamol (>1 dose), corticosteroids, 155

chest physiotherapy, CXR, RSV testing, and inflammatory blood tests. Inflammatory blood 156

tests included determination of C-reactive protein (CRP) levels and/or full blood counts (FBC) 157

and/or procalcitonin (PCT) levels. 158

To evaluate whether the HUGO guidelines affected the provision of supportive 159

treatments, we assessed the duration and the level of oxygen supplementation, as well as 160

the duration and the type of fluid replacement. Based on the nature of French bacterial 161

ecology, the HUGO guidelines recommend choosing amoxicillin in case of a concomitant 162

bacterial infection. We therefore evaluated the type of antibiotic that was prescribed. 163

Balancing measures to observe unintended consequences of the guidelines were: LOS, ICU 164

transfer, readmission at seven days, and mortality rates. 165

Statistical Analyses 166

The sample size was calculated on the basis of an expected reduction post-guidelines 167

implementation of 40% of the primary outcome, as published previously in other studies [6–168

8]. Assuming a power of 80%, α of 0.05, and a two-tailed test, the estimated sample size was 169

111 patients per period. This size was compatible with the approximately 150 bronchiolitis 170

hospitalizations at the NUH during three bronchiolitis epidemic weeks [13]. 171

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Continuous variables were expressed as medians and interquartile ranges (IQR) if 172

their distribution was abnormal, and the Mann-Whitney test was used. If the distribution was 173

normal, means, standard deviations, and the t-test were used. Categorical factors were 174

expressed as percentages, and they were compared using the χ2 tests. The Fisher’s test was 175

used if the expected numbers were <5. 176

Cost savings following implementation of the guidelines were obtained by determining 177

the difference between the mean cost per patient in 2011 and in 2013, and the standard error 178

of the difference in these means. Statistical analyses were performed using STATISTICA 179

version 10 software (data analysis software system StatSoft, Inc., 2011). 180

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RESULTS 181

During the inclusion periods, there were 638 emergency consultations for bronchiolitis 182

followed by 376 hospitalizations at the NUH. Of these patients, 311 were assessed for 183

eligibility for the study, and 280 patients were enrolled: 115 patients for period 1 (i.e. the 184

winter of 2011–2012) and 165 patients for period 2 (i.e. the winter of 2013–2014) (Fig 1). The 185

hospitalization rate following emergency consultation for bronchiolitis was higher in the winter 186

of 2013–2014 than in the winter of 2011–2012 (p<0.001). There was no significant difference 187

in the proportion of initial hospitalizations in the ICU for bronchiolitis between the two periods 188

(p=0.14). There were no significant differences between period 1 and period 2 group 189

characteristics, except in terms of the history of prematurity <37 SA (Table 1). 190

Primary Outcome 191

One year after implementation of the HUGO guidelines, the proportion of patients having at 192

least one treatment in conjunction with any of the tests was significantly reduced by two-193

thirds (Table 2). 194

Secondary Outcomes 195

In period 2, we noticed significant reductions in the use of CXRs and inflammatory blood 196

tests, as well as antibiotic and corticosteroids use. Downward trends for RSV testing and 197

oxygen supplementation were also observed (Table 2). Following implementation of the 198

guidelines, the prescription of amoxicillin-clavulanic acid declined, whereas prescription of 199

amoxicillin increased significantly. The use of chest physiotherapy, already minor in period 1, 200

was nearly absent in period 2. There was a switch from IV to nasogastric fluid administration 201

between periods 1 and 2. 202

In the subgroup analysis excluding patients with a history of prematurity (Online 203

Resource 1), and or those with comorbity (Online Resource 2), all of the differences that 204

were statistically significant in the general outcomes analysis remained significant. The 205

downward trends of IV and supplemental oxygen use became significant. 206

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The mean total cost of hospitalization per patient in the winter of 2011–2012 was 207

1,710.45€, and 1,656.40€ in the winter of 2013–2014. There were statistically significant 208

decreases in the mean laboratory costs and in the mean imaging costs between periods 1 209

and 2 (Table 3). 210

We found no difference in the rates of balancing measures after implementation of 211

the guidelines. The median LOS was 2.0 days with an interquartile range of 1.5 to 3.0 days in 212

period 1 and 2 (p=0.28). The ICU transfer rate was 6.96% in the winter of 2011–2012 and 213

4.24% in the winter of 2013–2014 (p=0.23). The readmission rate at seven days for all 214

causes was 4.35% prior to implementation of the HUGO guidelines, and 4.24% after their 215

implementation (p=0.59). There were no deaths during either period. 216

217

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DISCUSSION 218

This work is the first French study assessing the impact of a recent set of bronchiolitis 219

inpatient management guidelines. We showed that standardization of bronchiolitis inpatient 220

management allowed for a reduction in unnecessary treatments. One year after the 221

implementation of these guidelines, we noticed significant reductions in the use of CXR, 222

inflammatory blood tests, antibiotics, corticosteroids, and chest physiotherapy, without a 223

discernible increase in morbidity. The most recent AAP bronchiolitis guidelines reaffirm that 224

current evidence does not support routine use of CXR [4], and these should be reserved for 225

cases of ICU admission or signs of an airway complication such as pneumothorax. Carsin et 226

al. reported that, in France, the rate of differential diagnoses made thanks to CXR in 227

bronchiolitis was 0.08% [16]. It is important to remember that administering CXR is not 228

without potential for causing harm. Several studies suggest that CXR use in bronchiolitis 229

increases the prescription of antibiotics [17,18]. 230

The LOS of 2.0 days in our pragmatic study is similar to the 1.8 day LOS post-231

implementation of the guidelines as reported by Mittal and Ralston [7,10]. In France, a 232

national PMSI analysis of 29,784 children less than one year of age who were hospitalized 233

for bronchiolitis showed a median LOS of 3.0 days [1], similar to the LOS determined by 234

Carsin [16]. 235

In regard to supportive care, the downward trend of supplemental oxygen use that 236

was close to significance (p=0.058) can probably be explained by the reduction of the 237

supplemental oxygen introduction limit at SpO2 < 92% (<95% if associated with signs of 238

severity), and the promotion of discontinuous pulse oxymetry by the HUGO guidelines. The 239

absence of a decrease in the duration of oxygen supplementation in our work may be linked 240

to the oxygen discontinuation criteria (SpO2 >92% when asleep, >94% when awake). These 241

criteria could be reassessed, particularly in light of the results of the randomized, controlled 242

equivalence trial of Cunningham et al. that revealed an SpO2 of ≥90% as being as safe and 243

clinically effective as one of ≥94% [19]. 244

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Economic improvement was not the aim of the HUGO guidelines, and their 245

implementation allowed for little cost savings, especially in terms of laboratory tests and 246

imaging costs. 247

We did not observe any significantly adverse effects of the HUGO bronchiolitis 248

guidelines on mortality, ICU transfers, or readmission rates at seven days, but this could be 249

due to the fact that our study lacked the power to adequately evaluate this. However, 250

previously published studies involving larger populations that evaluated the impact of similar 251

bronchiolitis guidelines, did not report any deleterious effects on morbidity [6,7,9]. 252

253

The main limitation of this study was its retrospective, monocentric before vs. after 254

design. Nevertheless, it is important to note that no international bronchiolitis guidelines were 255

published between December 2011 and January 2014. In order to limit bias, we choose to 256

evaluate the same unit during the three major bronchiolitis epidemic weeks. We 257

hypothesized that the workload is similar year-over-year during those periods. There was no 258

major change in the way the unit was run, senior medical staff, or nurse teams between the 259

two inclusion periods. There was no significant difference between the baseline 260

characteristics of the two periods for the populations hospitalized in the general pediatric unit, 261

except for in terms of their history of prematurity. However, this difference appeared to have 262

a minor impact on our study’s outcomes. Indeed, in the subgroup analysis that excluded 263

patients with a history of prematurity, all of the statistically significant differences in the 264

general outcomes analysis remained significant. 265

Even though our study was monocentric, the characteristics of our population are 266

similar to those of other published studies, particularly in three recent studies conducted in 267

others French university hospitals [16,20,21]. These rates, as those reported in the study of 268

the ESPID [11], are higher in comparison to those of our period 2. They could probably be 269

improved through implementation of the bronchiolitis guidelines. 270

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Lastly, although our study was retrospective, it was exhaustive. Indeed, our outcomes 271

were routine treatments that were well documented in the medical files, and we limited the 272

selection bias through PMSI use. 273

274

In comparison to the results of other quality improvement studies, such as those 275

reported in Ralston’s systematic review [9], we encountered better reduction rates for 276

unnecessary diagnostic tests and treatments. This level of success is probably linked to the 277

design of our intervention, as it was a voluntary local collaborative work. Indeed the 278

collaborative nature of the work helps to overcome clinical practice inertia and to promote 279

evidence based medicine [22]. These determinants of successful deimplementation should 280

be specifically targeted when the upcoming national French bronchiolitis guidelines are set 281

up in the near future across the country. Further research is needed to assess if the 282

deimplementation of the unnecessary treatments is sustained over time, and can be 283

broadened at other hospitals, especially in the community hospitals. 284

285

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CONTRIBUTORS 286

MB, CG, MV and EL designed the study. EL and CG supervised the study. MB was 287

responsible for the data collection. MB and CG performed the data analysis. MB wrote the 288

first draft of the manuscript. .All authors interpreted the data, contributed to writing and 289

revising the manuscript and take full responsibility for the integrity of the data and the 290

accuracy of the data analysis. 291

ACKNOWLEDGMENTS 292

We thank Arnaud Legrand for his statistical guidance, Noemie Fortin and Bruno Hubert from 293

the French Institute for Public Health of the Pays de la Loire for their help with retrieving 294

epidemiologic data, and Nathalie Surer and Marion Le Moal for their support of the PMSI 295

extraction and the costs study. We are grateful to the patients and their families. We thank all 296

of the physicians and nurses for their proper management of the medical files. 297

FUNDING 298

This research received no specific grant from any funding agency in the public, commercial 299

or not-for-profit sectors 300

301

COMPETING INTERESTS 302

The authors have no conflicts of interest to disclose. All authors declare: no support from any 303

organisation for the submitted work; no financial relationships with any organisations that 304

might have an interest in the submitted work in the previous three years, no other 305

relationships or activities that could appear to have influenced the submitted work. 306

ETHICS APPROVAL 307

The project was approved by the institutional review board at the Nantes University Hospital, 308

and was in accordance with the 1964 Helsinki declaration and its later amendments or 309

comparable ethical standards. French legislation stipulates that informed consent is not 310

required and local retrospective data may be used for an epidemiologic study. 311

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Myriam Benhamida affirms that the manuscript is an honest, accurate, and transparent 312

account of the study being reported; that no important aspects of the study have been 313

omitted; and that any discrepancies from the study as planned have been explained 314

DATA SHARING STATEMENT 315

Relevant anonymised data are available on reasonable request from the corresponding 316

author. 317

318

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7 Mittal V, Darnell C, Walsh B, et al. Inpatient Bronchiolitis Guideline Implementation and 336

Resource Utilization. Pediatrics 2014;133:e730–7. 337

8 Parikh K, Hall M, Teach SJ. Bronchiolitis Management Before and After the AAP 338

Guidelines. Pediatrics 2014;133:e1–7. 339

9 Ralston S, Comick A, Nichols E, et al. Effectiveness of Quality Improvement in 340

Hospitalization for Bronchiolitis: A Systematic Review. Pediatrics 2014;134:571–81. 341

10 Ralston SL, Garber MD, Rice-Conboy E, et al. A Multicenter Collaborative to Reduce 342

Unnecessary Care in Inpatient Bronchiolitis. Pediatrics 2016;137:1–9. 343

11 Carande EJ, Pollard AJ, Drysdale SB. Management of Respiratory Syncytial Virus 344

Bronchiolitis: 2015 Survey of Members of the European Society for Paediatric Infectious 345

Diseases. Can J Infect Dis Med Microbiol 2016;2016. 346

12 Verstraete M, Cros P, Gouin M, et al. Prise en charge de la bronchiolite aiguë du 347

nourrisson de moins de 1 an : actualisation et consensus médical au sein des hôpitaux 348

universitaires du Grand Ouest (HUGO). Arch Pédiatrie 2014;21:53–62. 349

13 Fortin N. Epidémies de bronchiolite dans l’agglomération nantaise 2007-2012. 2015. 350

http://opac.invs.sante.fr/doc_num.php?explnum_id=10178. 351

14 Howell V, Schwartz AE, O’Leary JD, et al. The effect of the SQUIRE (Standards of 352

QUality Improvement Reporting Excellence) guidelines on reporting standards in the 353

quality improvement literature: a before-and-after study. BMJ Qual Saf 2015;24:400–6. 354

15 Florin TA, Plint AC, Zorc JJ. Viral bronchiolitis. The Lancet 2017;389:211–24. 355

16 Carsin A, Gorincour G, Bresson V, et al. La radiographie de thorax chez le nourrisson 356

hospitalisé pour bronchiolite aiguë : réelle information ou simple irradiation ? Arch 357

Pédiatrie 2012;19:1308–15. 358

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17 Schuh S, Lalani A, Allen U, et al. Evaluation of the Utility of Radiography in Acute 359

Bronchiolitis. J Pediatr 2007;150:429–33. 360

18 Swingler GH, Hussey GD, Zwarenstein M. Randomised controlled trial of clinical 361

outcome after chest radiograph in ambulatory acute lower-respiratory infection in 362

children. The Lancet 1998;351:404–8. 363

19 Cunningham S, Rodriguez A, Adams T, et al. Oxygen saturation targets in infants with 364

bronchiolitis (BIDS): a double-blind, randomised, equivalence trial. Lancet Lond Engl 365

2015;386:1041–8. 366

20 Arnoux V, Carsin A, Bosdure E, et al. Radiographie de thorax et bronchiolite aiguë : des 367

indications en diminution ? Arch Pédiatrie 2017;24:10–6. 368

21 Gajdos V, Katsahian S, Beydon N, et al. Effectiveness of Chest Physiotherapy in Infants 369

Hospitalized with Acute Bronchiolitis: A Multicenter, Randomized, Controlled Trial. PLOS 370

Med 2010;7:e1000345. 5 371

22 Cabana MD, Rand CS, Powe NR, et al. Why don’t physicians follow clinical practice 372

guidelines?: A framework for improvement. JAMA 1999;282:1458–65. 373

374

375

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TABLES 376

TABLE 1 Baseline Patient Characteristics

2011 n = 115 2013 n = 165 P value

Age, months, mean ± SD 2.70 ± 2.57 2.17 ± 2.23 0.07

Gender, male 64/115 (55.65%) 89/165 (53.94%) 0.78

History wheezing =1 12/115 (10.43%) 15/165 (9.09 %) 0.71

Comorbidity 13/115 (11.30 %) 11/165 (6.67 %) 0.17

Prematurity < 37 SA 14/115 (12.17 %) 8 /165 (4.85 %) 0.03

377

378

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379

TABLE 2 Outcomes Pre- and Post H.U.G.O Guideline Implementation

2011 n = 115 2013 n = 165 P value

Treatmentᵃ and test ᵇ 52/115 (45.22%) 25/165 (15.15%) < 0.001

At least 1 treatment 52/115 (45.22%) 46/165 (27.88%) 0.003

At least 1 test ᵇ 101/115 (87.83%) 52/165 (31.52) < 0.001

CXR 99/115 (86.09%) 44/165 (26.67%) < 0.001

RSV Nasopharyngeal swabs 28/115 (24.35%) 26/165 (15.76%) 0.073

Inflammatory Blood test 34/115 (29.57%) 18/165 (10.91%) < 0.001

Antibiotic use 44/115 (38.26%) 22/165 (13.33%) < 0.001

Salbutamol use > 1 dose 9/115 (8.0%) 8/165 (5.0%) 0.213

Corticosteroid use 12/115 (10.43%) 5/165 (3.03%) 0.011

Chest Physiotherapy 7/115 (6.09%) 1/165 (0.61%) 0.009

Nasogastric fluid replacement 19/115 (16.52%) 58/165 (35.15%) < 0.001

Nasogastric feed lenght, d, median

(IQR) 1.5 (1.0-3.0) 2.0 (1.0-3.0) 0.698

IV fluid replacement 25/115 (21.74%) 22/165 (13.33%) 0.064

IV hydratation length, d, median (IQR) 1.0 (1.0-1.5) 1.5 (0.5-2.0) 0.592

Oxygen use 71/115 (61.74%) 83/165 (50.30%) 0.058

O2 max, L/min, median (IQR) 0.5 (0.25-1) 0.5 (0.5-1) 0.667

Oxygen lenght, d, median (IQR) 2.0 (1.0-2.5) 2.0 (1.5-3.0) 0.103

% amoxicillin in ATB 9/44 (20.45%) 19/22 (86.36%) <0.001

% amoxicillin-clavulanic acid in ATB 28/44 (63.63%) 1/22 (4.54%) <0.001

ᵃ Treatment among antibiotics /salbutamol / corticosteroids

ᵇ Test among CXR / blood test / RSV test CXR, chest -X-ray; RSV, respiratory syncytial virus; ATB, antibiotic prescription ; IV, intravenous, IQR, interquartile range 380

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TABLE 3 Cost Saving per Patient Post Guideline Implementation

Mean cost saving per patient, €, ± SE P value

Laboratory test -26.12 ± 7.80 0.003

Imagery -17.77 ± 2.63 <0.001

Material and supplies -28.03 ± 16.99 0.082

Drugs -14.15 ± 12.19 0.24

Global unit functioning 40.71 ± 126.00 0.80

381

382

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FIGURE CAPTION 383

Fig. 1 Study population flow diagram 384

Footnotes : GP unit, general pediatric; InVs, French Institut for Public Health ; ICU, intensive 385

care unit. 386

387

388

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195x176mm (96 x 96 DPI)

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ONLINE RESOURCE 1

BRONCHIOLITIS: KEEP IT SIMPLE, A FRENCH EXPERIMENT

EUROPEAN JOURNAL OF PEDIATRICS

BENHAMIDA M, BIHOUEE T, VERSTRAETE M, GRAS LE GUEN C, LAUNAY E.

Oneline Resource 1 Outcomes Pre- and Post H.U.G.O Guideline Implementation

Sub Group Analysis without patients with prematurity history

2011 n = 101 2013 n = 157 P value

Treatment ᵃ and test ᵇ 47/101 (45.22%) 23/157 (14.65%) < 0.001

At least 1 treatment 45/101 (44.55%) 43/157 (27.39%) <0.001

At least 1 test ᵇ 90/101 (89.11%) 50/157 (31.85%) < 0.001

CXR 89/101 (88.12%) 43/157 (27.39%) < 0.001

RSV Nasopharyngeal swabs 24/101 (23,76%) 25/157 (15.92%) 0.117

Inflammatory Blood test 30/101 (29,70%) 17/157 (10.83%) 0.001

Antibiotic use 39/101 (38.61%) 21/157 (13.38%) < 0.001





I.V. fluid replacement 24/101 (23.76%) 21/157 (13.68%) 0.032

Oxygen use 66/101 (65.35%) 78/157 (49.68%) 0.013

O2 max, L/min, median (IQR) 0.5 (0.25-1.0) 0.5 (0.25-2.0) 0.64


LOS in GP unit, d, median (IQR) 2.5 (1.5-3.5) 2,5 (1.5-3.5) 0.73

ICU transfer 8/101 (7.92%) 7/157 (4.46%) 0.19

All-cause 7-day readmission 5/101 (4.95%) 7/157 (4.46%) 0.54

Treatment among antibiotics /salbutamol / corticosteroids

ᵇ Test among CXR / blood test / RSV test

CXR, chest -X-ray; RSV, respiratory syncytial virus; ATB, antibiotic prescription ;

IV, intravenous; IQR, interquartile range

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ONLINE RESOURCE 2

BRONCHIOLITIS: KEEP IT SIMPLE, A FRENCH EXPERIMENT

EUROPEAN JOURNAL OF PEDIATRICS



Sub Group Analysis without patients with comorbidities

2011 n = 102 2013 n = 154 P value

Treatment ᵃ and test ᵇ 42/102 (41.18%) 23/154 (14.94%) < 0,001

At least 1 treatment 45/102 (41.18%) 42/154 (27.27%) < 0,001

At least 1 test ᵇ 89/102 (87.25%) 47/154 (31,85%) < 0,001

CXR 86/102 (84.34%) 47/154 (30.52%) < 0,001

RSV Nasopharyngeal swabs 28/102 (27.45%) 22/154 (14.29%) 0,073

Inflammatory Blood test 30/102 (29.41%) 15/154 (9.74%) < 0,001

Antibiotic use 38/102 (37.25%) 22/154 (14.29%) < 0,001

Salbutamol use > 1 dose 8/102 (7.84%) 7/154 (4.55%) 0,28

Corticosteroid use 10/102 (9.80%) 5/154 (3.25%) 0,013

Chest Physiotherapy 6/102 (5.88%) 0/154 (0%) 0,009

Nasogastric fluid replacement 15/102 (14.71%) 56/154 (36.36%) < 0,001

I.V. fluid replacement 22/102 (21,59%) 19/154 (12.34%) 0,049

Oxygen use 65/102 (65,69%) 76/154 (49.35%) 0,01

O2 max, L/min, median (IQR) 0.5 (0,25-1.0) 0.5 (0,25-2.0) 0,54

Oxygen lenght, d, median (IQR) 1.5 (1.0-2.5) 1.5(1.5-3.0) 0,19

LOS in GP unit, d, median (IQR) 2.0 (1,5-3.5) 2.0 (1,5-3,5) 0,37

ICU transfer 7/102 (6.86%) 4/154 (2.60%) 0,23

All-cause 7-day readmission 4/102 (3.92%) 7/154 (4.55%) 0,59





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RETROSPECTIVE AUDIT OF GUIDELINES FOR

INVESTIGATION AND TREATMENT OF BRONCHIOLITIS: A

FRENCH PERSPECTIVE


Manuscript ID bmjpo-2017-000089.R1


Date Submitted by the Author: 22-Jun-2017






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TITLE PAGE 1

TITLE: 2

RETROSPECTIVE AUDIT OF GUIDELINES FOR INVESTIGATION AND TREATMENT OF 3

BRONCHIOLITIS: A FRENCH PERSPECTIVE 4

AUTHORS: 5







¹Clinique Médicale de Pédiatrie, Hôpital Mère Enfant, Centre Hospitalier Universitaire Nantes, 12

7 quai Moncousu 44093, Nantes Cedex 1, France 13


Adress : Clinique Médicale de Pédiatrie, CHU de Nantes, 7 quai Moncousu 44093, Nantes Cedex 1, France 15

Phone : +33 2.40.08.44.54 16


the Corresponding Author has the right to grant on behalf of all authors and does grant on behalf of all authors, 18

an exclusive licence on a worldwide basis to the BMJ Publishing Group Ltd to permit this article to be published 19

in BMJ editions and any other BMJPGL products and sublicences such use and exploit all subsidiary rights, as 20

set out in our licence. 21

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The results of this study were presented at the annual meeting of the French Pediatric Society in May 2016 in 22

Lille (France) 23

ABSTRACT 24

(i) As the most recent French bronchiolitis guidelines were published in 2000, there is a current over-25

investigation and an over-treatment of infants hospitalized with bronchiolitis in France. In 2012, the Group of 26

Pediatric University Hospitals in Western France (‘HUGO’) proposed new evidence-based clinical practice 27

guidelines in keeping with the latest international guidelines.The aim study was to determine the impact of these 28

guidelines on the management of bronchiolitis inpatients. 29

(ii) This retrospective before after design study was conducted in the general pediatric unit of a tertiary level of 30

care French hospital, either one year before (i.e. the winter of 2011-2012) or one year after (i.e. the winter of 31

2013-2014) implementation of the guidelines. 280 bronchiolitis inpatients, less than one year of age, were 32

included. The primary outcome was the proportion of children administered a diagnostic test associated with a 33

treatment not routinely recommended by the guidelines. As balancing measures we evaluated the length of stay, 34

the ICU transfer and the readmission rates. 35

(iii) Following implementation of the guidelines, use of any given treatment associated with a diagnostic test was 36

reduced by 66% (p<0.001). There were major decreases in the use of chest-X-ray (86% vs 26%, p<0.001), 37

antibiotics (38.23% vs 13.33%, p<0.001), and corticosteroids (10.43% vs 3.03%, p=0.011). Balancing measures 38

were not significantly different. 39

(iv) HUGO guidelines were effective at reducing the administration of unnecessary diagnostic tests and 40

medications. This study was the first step to convince the French pediatricians to streamline their practices until 41

the publication of updated national bronchiolitis guidelines. 42

43

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What is known about the subject 44

• Bronchiolitis results in 30.000 hospitalizations annually in France, where the most recent guidelines on 45

the subject date from 2000. 46

• There is a current overuse of diagnostic and therapeutic resources in the management of bronchiolitis 47

inpatient in France. 48

• Ralston et al. have proposed as achievable benchmarks of cares (ABCs) for inpatients care in 49

bronchiolitis. 50

What this study adds 51

• This work is the first French study assessing the impact of a recent set of bronchiolitis inpatient 52

management guidelines. 53

• Reducing the administration of unnecessary diagnostic tests and medications, especially chest-X-ray 54

prescription and chest physiotherapy on a French population is possible. 55

• No discernible adverse effect was observed. 56

57

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ABREVIATIONS 58

ABC Achievable Benchmarks of Cares




CXR Chest X-ray







LOS Length of stay



PCT Procalcitonin



59

60

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TEXT 61

INTRODUCTION 62

Acute viral bronchiolitis results in 30,000 hospitalizations annually in France [1]. But, while in 2014 and 2015 63

the National Institute for Health and Care Excellence (NICE)[2], the American Academy of Pediatrics (AAP)[3], 64

and the Canadian Pediatric Society (CPS) [4], recommend curtailing the excessive use of antibiotics, chest X-65

rays (CXR), respiratory syncytial virus (RSV) testing, inflammatory blood test, as well as unnecessary 66

treatments such as the administration of corticosteroids, salbutamol, and chest physiotherapy; the most recent 67

French guidelines date from 2000[5]. This was leading to a current overinvestigation and an overtreatment of 68

infants hospitalized with bronchiolitis in our country. Thus, in two recent French studies[6,7], the rates of CXR, 69

RSV testing and inflammatory blood testing performed were between 59.3% and 97.8%, between 89.5% and 70

98.7%, and around 57.7%, respectively. In the study of Arnoux et al. the rate of chest physiotherapy raised 71

75%[7]. And in 2013, Gajdos et al. reported a 14% rate for salbutamol use, 10% for corticosteroids, and 28% for 72

antibiotics [8]. In comparison, Ralston et al. have proposed as achievable benchmarks of cares (ABCs) for 73

inpatients care in bronchiolitis[9]: a 10-19% rate of use for bronchodilatators, a 0-9% rate of use for 74

corticosteroids, a 17-19% rate of use for antibiotics, and a 31-42% rate of use for CXR. And in a study 75

conducted in 17 American hospital, in 2010, the rate of chest physiotherapy was 4% [10]. In addition, the rate of 76

antibiotics use and RSV testing were 10% and 29%, in the study of Akenroy et al. [11]. 77

In order to improve bronchiolitis inpatient management, the Group of Pediatric University Hospitals in Western 78

France (‘HUGO’) published guidelines in 2012 [12], that are in keeping with the latest international 79

recommendations. In this study we sought to determine the impact of these HUGO guidelines. Our primary aim 80

was to evaluate whether streamlining of practices could be implemented in France. We hypothesized that the 81

proportion of patients receiving treatments such as antibiotics, corticosteroids, or salbutamol, and a diagnostic 82

test such as chest X-rays, respiratory syncytial virus (RSV) testing, or a blood test would be reduced following 83

implementation of the HUGO guidelines. As secondary outcomes, we evaluated the length of stay (LOS), 84

hospitalization costs, and rates of intensive care unit (ICU) transfer and readmission at seven days. We also 85

compared the modalities of supportive care prior to and following implementation of the guidelines. 86

87

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METHODS 88


The Nantes University Hospital (NUH) provides pediatric care for a geographical area with a population of 90

850,000 with 12,107 births in 2010. Every winter, bronchiolitis accounts for approximately 500 hospitalizations 91

at the NUH [13]. We conducted a retrospective study of quality improvement intervention in order to standardize 92

the care provided to bronchiolitis inpatients. We compared the year prior to implementation of the HUGO 93

guidelines (i.e. the winter of 2011-2012) to the year following their implementation (i.e. the winter of 2013-94

2014). We deemed the winter of 2012-2013 to be a transition year. 95

For each bronchiolitis season, we analyzed the three weeks of major bronchiolitis epidemics. Every year, during 96

those weeks, the NUH general pediatric unit becomes overcrowded, accommodating essentially just bronchiolitis 97

inpatients. We hypothesized that the workload is similar year-over-year during those periods. According to the 98

regional office of the French Institute for Public Health of the Pays de la Loire, for the winter of 2011–2012, the 99

three major bronchiolitis epidemic weeks were weeks 48, 49, and 50. For the winter of 2013–2014 they were 100

weeks 51, 52, and 1. 101


We followed SQUIRE guidelines to report this study [14]. French legislation stipulates that informed consent is 103

not required and local retrospective data may be used for an epidemiologic study. 104

Intervention: HUGO Bronchiolitis Guidelines Development and Implementation 105

In 2011, the pediatricians, pediatric pulmonologists, and emergency physicians belonging to HUGO met to 106

analyze the recent published data regarding bronchiolitis in children less than one year of age. Criteria to 107

distinguish childhood asthma from acute viral bronchiolitis were established. Prescriptions of diagnostic tests, 108

antibiotics, and chest physiotherapy were defined and reserved for limited situations. Modalities of oxygen 109

supplementation and nutritional support were proposed. All these recommendations were summarized in the 110

HUGO bronchiolitis guidelines[12]. 111

The guidelines were implemented by the NUH in September 2012, by holding team meetings involving pediatric 112

nurses, physicians, and trainees. These interprofessional meetings take place every year at the start of 113

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bronchiolitis season. The guidelines were integrated into the NUH guidelines book, and they are readily 114

accessible online via the hospital’s intranet website. 115


The target population for the HUGO bronchiolitis guidelines was children from birth to one year of age, who 117

were diagnosed with bronchiolitis. The diagnosis of bronchiolitis was based on their medical history and a 118

physical examination showing viral upper respiratory tract prodrome, followed by increased respiratory effort 119

and wheezing, as recommended in the HUGO and international guidelines [3,12,15,16]. 120

Using the NUH Medical Program of Information System (PMSI), we screened for all patients with a 121

bronchiolitis diagnosis defined by the group of codes “Acute Bronchiolitis” of the International Classification of 122

Disease 10 (J21, J21.0, J21.8, J21.9), and who were hospitalized in the general pediatric unit of the NUH during 123

the inclusion periods. Of these patients, we excluded patients aged >12 months old, patients with a history of 124

more than one wheezing dyspnea episode, and obvious mistakes in the PMSI such as an absence of any clinical 125

signs of respiratory infection in their medical files. 126

We opted for a pragmatic study, so we did not exclude patients with comorbidities or those that had required a 127

transfer to the ICU at any time during their management. Only the patient’s management in the general pediatric 128

unit was evaluated. 129

Data were collected by the retrospective review of medical files, and tabulated using Excel (Microsoft, Inc, 130

Redmond, USA). Data on the cost of services were obtained from the hospital’s administrative and financial 131

databases for each included patient. 132


To capture the overall impact of the HUGO guidelines, we used a composite outcome build with the two main 134

resources that tend to be misused in bronchiolitis: diagnostic tests and treatments. Our primary outcome was the 135

proportion of patients having been administered at least one antibiotic, corticosteroid, or salbutamol treatment, 136

and either a CXR, RSV testing, or an inflammatory blood test. We selected these treatments and tests because 137

their use is not routinely recommended by the HUGO guidelines. Moreover, they are typical outcomes used to 138

evaluate unnecessary treatments in bronchiolitis quality improvement studies [9,11,17,18]. 139

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As secondary outcomes, we compared total hospitalization costs (including the cost of overall unit functioning, 140

laboratory tests, imaging, drugs, supplies, and materials), the use of each treatment and diagnostic test: 141

antibiotics, salbutamol (>1 dose), corticosteroids, chest physiotherapy, CXR, RSV testing, and inflammatory 142

blood tests. Inflammatory blood tests included determination of C-reactive protein (CRP) levels and/or full blood 143

counts (FBC) and/or procalcitonin (PCT) levels. 144

To evaluate whether the HUGO guidelines affected the provision of supportive treatments, we assessed the 145

duration and the level of oxygen supplementation, as well as the duration and the type of fluid replacement. 146

Indeed, the guidelines suggest limiting continuous pulse oxymetry; decreasing oxyhemoglobin saturation (SpO2) 147

targets, especially during sleep; and nasogastric feeding is preferred, with the exception of severe bronchiolitis in 148

patients with a WANG score > 8. Based on the nature of French bacterial ecology, especially for Haemophilus 149

influenzae, the HUGO guidelines recommend choosing amoxicillin in case of a concomitant bacterial infection. 150

We therefore evaluated the type of antibiotic that was prescribed. Balancing measures to observe unintended 151

consequences of the guidelines were: LOS, ICU transfer, readmission at seven days, and mortality rates. 152


The sample size was calculated on the basis of an expected reduction post-guidelines implementation of 40% of 154

the primary outcome, as published previously in other studies [11,17,19]. Assuming a power of 80%, α of 0.05, 155

and a two-tailed test, the estimated sample size was 111 patients per period. This size was compatible with the 156

approximately 150 bronchiolitis hospitalizations at the NUH during three bronchiolitis epidemic weeks [13]. 157

Continuous variables were expressed as medians and interquartile ranges (IQR) if their distribution was 158

abnormal, and the Mann-Whitney test was used. If the distribution was normal, means, standard deviations, and 159

the t-test were used. Categorical factors were expressed as percentages, and they were compared using the χ2 160

tests. The Fisher’s test was used if the expected numbers were <5. 161

Cost savings following implementation of the guidelines were obtained by determining the difference between 162

the mean cost per patient in 2011 and in 2013, and the standard error of the difference in these means. Statistical 163

analyses were performed using STATISTICA version 10 software (data analysis software system StatSoft, Inc., 164

2011). 165

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RESULTS 166

During the inclusion periods, there were 638 emergency consultations for bronchiolitis followed by 376 167

hospitalizations at the NUH. Of these patients, 311 were assessed for eligibility for the study, and 280 patients 168

were enrolled: 115 patients for period 1 (i.e. the winter of 2011–2012) and 165 patients for period 2 (i.e. the 169

winter of 2013–2014) (Fig 1). The hospitalization rate following emergency consultation for bronchiolitis was 170

higher in the winter of 2013–2014 than in the winter of 2011–2012 (p<0.001). There was no significant 171

difference in the proportion of initial hospitalizations in the ICU for bronchiolitis between the two periods 172

(p=0.14). There were no significant differences between period 1 and period 2 group characteristics, except in 173

terms of the history of prematurity <37 SA (Table 1). 174

Primary Outcome 175

One year after implementation of the HUGO guidelines, the proportion of patients having at least one treatment 176

in conjunction with any of the tests was significantly reduced by two-thirds (Table 2). 177


In period 2, we noticed significant reductions in the use of CXRs and inflammatory blood tests, as well as 179

antibiotic and corticosteroids use. Downward trends for RSV testing and oxygen supplementation were also 180

observed (Table 2). Following implementation of the guidelines, the prescription of amoxicillin-clavulanic acid 181

declined, whereas prescription of amoxicillin increased significantly. The use of chest physiotherapy, already 182

minor in period 1, was nearly absent in period 2. There was a switch from IV to nasogastric fluid administration 183

between periods 1 and 2. The durations of IV or nasogastric fluid replacement were not different prior to and 184

following implementation of the HUGO guidelines. 185

In the subgroup analysis excluding patients with a history of prematurity (Online Resource 1), and or those with 186

comorbity (Online Resource 2), all of the differences that were statistically significant in the general outcomes 187

analysis remained significant. The downward trends of IV and supplemental oxygen use became significant. 188

The mean total cost of hospitalization per patient in the winter of 2011–2012 was 1,710.45€, and 1,656.40€ in 189

the winter of 2013–2014. There were statistically significant decreases in the mean laboratory costs and in the 190

mean imaging costs between periods 1 and 2 (Table 3). 191

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We found no difference in the rates of balancing measures after implementation of the guidelines. The median 192

LOS was 2.0 days with an interquartile range of 1.5 to 3.0 days in period 1 and 2 (p=0.28). The ICU transfer rate 193

was 6.96% in the winter of 2011–2012 and 4.24% in the winter of 2013–2014 (p=0.23). The readmission rate at 194

seven days for all causes was 4.35% prior to implementation of the HUGO guidelines, and 4.24% after their 195

implementation (p=0.59). There were no deaths during either period. 196

197

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DISCUSSION 198

This work is the first French study showing, standardization of bronchiolitis inpatient management, allowed for a 199

reduction in unnecessary testings and treatments. One year after the implementation of these guidelines, we 200

noticed significant reductions in the use of CXR, inflammatory blood tests, antibiotics, corticosteroids, and chest 201

physiotherapy, without a discernible increase in morbidity. Thus the ABCs for inpatients care in bronchiolitis 202

proposed by Ralston et al. were reached [9]. 203

The main limitation of this study was its retrospective, monocentric before vs. after design. In order to limit bias, 204

we choose to evaluate the same unit during the three major bronchiolitis epidemic weeks. We hypothesized that 205

the workload is similar year-over-year during those periods. There was no major change in the way the unit was 206

run, senior medical staff, or nurse teams between the two inclusion periods. There was no significant difference 207

between the baseline characteristics of the two periods for the populations, except for in terms of their history of 208

prematurity. For this characteristic, the rate for period 1 of 12.17% was similar to the finding in other studies 209

with rates between 8.7 and 16% [6,20]. However, this difference appeared to have a minor impact on our study’s 210

outcomes. Indeed, in the subgroup analysis that excluded patients with a history of prematurity, all of the 211

statistically significant differences in the general outcomes analysis remained significant. We did not observe 212

any significantly adverse effects of the HUGO bronchiolitis guidelines on mortality, ICU transfers, or 213

readmission rates at seven days, but this could be due to the fact that our study lacked the power to adequately 214

evaluate this. However, previously published studies involving larger populations that evaluated the impact of 215

similar bronchiolitis guidelines did not report any deleterious effects on morbidity [11,18,19]. 216

Even though our study was monocentric, the characteristics of our population are similar to those of other 217

published studies, particularly in three recent studies conducted in others French university hospitals [6–8]. In 218

the study of Carsin et al. [6], the rates of nasopharyngeal viral swabs, inflammatory blood tests, and IV fluid 219

replacements were 98.7%, 57.7%, and 54%, respectively. Gajdos et al. reported a 14% rate for salbutamol use, 220

10% for corticosteroids, and 28% for antibiotics [8]. 221

The current over-investigation and an over-treatment of infants hospitalized with bronchiolitis in France is not 222

without potential for causing harm. Chest physiotherapy had no significant effect on time to recovery [21], but 223

increased the frequency of vomiting and transitory respiratory destabilization in the work of Gadjos et al.[8]. 224

Concerning CXR, the NICE [2], the AAP [3] and the CPS bronchiolitis guidelines [16], reaffirm that current 225

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evidence does not support its routine use. It should be reserved for cases of ICU admission or signs of an airway 226

complication such as pneumothorax. Indeed, the rate of differential diagnoses made thanks to CXR in 227

bronchiolitis was between 0.4% and 0.8% in recent studies [6,22], whereas several studies suggest that CXR use 228

increases the prescription of antibiotics [22–24]. Schuh et al. showed the rate of infants identified for antibiotics 229

pre-radiography was 2.6%, and became 14.7% post-radiography [22]. Similarly, a French study showed 13.5% 230

of the children without CXR received antibiotics versus 38.8% of those with CXR [23]. And Carsin et al. 231

reported only 3.6% of the routinely performed CXR changed bronchiolitis inpatient management [6], almost all 232

by antibiotic introduction.In addition, reducing unnecessary cares provided benefits in term of LOS and costs 233

saving. AAP guidelines implementations were followed by reduction of the LOS from 2.3 to 1.8 days in Mittal’s 234

study[19], and from 2.0 to 1.8 day in Ralston’s study[25]. In our pragmatic study, the LOS remained stable at 2.0 235

days. But it should be kept in mind that those studies excluded patients transferred to the ICU or who had 236

comorbidities. Moreover in France, a national PMSI analysis of 29,784 children hospitalized for bronchiolitis 237

showed a median LOS of 3.0 days[1]. And the mean LOS observed in the recent multicentric French trial on 238

hypertonic saline nebulization, was 3.8 days [26]. Finally the implementation of HUGO guidelines allowed for 239

little cost savings of €54.25 per patient. In comparison, Akenroye et al. reported a mean cost per patient reduced 240

by $197[11]. In regard to supportive care, the downward trend of supplemental oxygen use that was close to 241

significance (p=0.058) can probably be explained by the reduction of the supplemental oxygen introduction limit 242

at SpO2 < 92% (<95% if associated with signs of severity), and the promotion of intermittent pulse oxymetry. 243

Concerning intermittent pulse oxymetry monitoring, a recent randomized trial confirmed it can be routinely used 244

in the management of bronchiolitis inpatients, who show clinical improvement [27]. The absence of a decrease 245

in the duration of oxygen supplementation in our work may be linked to the HUGO oxygen discontinuation 246

criteria (SpO2 >92% when asleep, >94% when awake). These criteria could be reassessed, particularly in light of 247

the results of the randomized, controlled equivalence trial of Cunningham et al. that revealed an SpO2 of ≥90% 248

as being as safe and clinically effective as one of ≥94% [28]. 249

In conclusion, we showed reducing the overuse of unnecessary diagnostic and therapeutic measure was possible 250

in France. This study was a first step to convince the French pediatricians still reluctant to streamline their 251

practices, before the upcoming national French bronchiolitis guidelines. 252

253

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CONTRIBUTORS 254

MB, CG, MV and EL designed the study. EL and CG supervised the study. MB was responsible for the data 255

collection. MB and CG performed the data analysis. MB wrote the first draft of the manuscript. .All authors 256

interpreted the data, contributed to writing and revising the manuscript and take full responsibility for the 257

integrity of the data and the accuracy of the data analysis. 258

ACKNOWLEDGMENTS 259

We thank Arnaud Legrand for his statistical guidance, Noemie Fortin and Bruno Hubert from the French 260

Institute for Public Health of the Pays de la Loire for their help with retrieving epidemiologic data, and Nathalie 261

Surer and Marion Le Moal for their support of the PMSI extraction and the costs study. We are grateful to the 262

patients and their families. We thank all of the physicians and nurses for their proper management of the medical 263

files. 264

FUNDING 265

This work was supported by any grant. 266


The authors have no conflicts of interest to disclose. All authors declare: no support from any organisation for 268

the submitted work; no financial relationships with any organisations that might have an interest in the submitted 269

work in the previous three years, no other relationships or activities that could appear to have influenced the 270

submitted work. 271

ETHICS APPROVAL 272

The project was approved by the institutional review board at the Nantes University Hospital, and was in 273

accordance with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. French 274

legislation stipulates that informed consent is not required and local retrospective data may be used for an 275

epidemiologic study. 276

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Myriam Benhamida affirms that the manuscript is an honest, accurate, and transparent account of the study being 277

reported; that no important aspects of the study have been omitted; and that any discrepancies from the study as 278

planned have been explained. 279


Relevant anonymised data are available on reasonable request from the corresponding author. 281

282

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REFERENCE 283

1 Che D, Caillère N, Josseran L. Surveillance et épidémiologie de la bronchiolite du nourrisson en France. 284

Arch Pédiatrie 2008;15:327–8. 285

2 Ricci V, Delgado Nunes V, Murphy MS, et al. Bronchiolitis in children: summary of NICE guidance. BMJ 286 2015;350:h2305–h2305. 287

3 Ralston SL, Lieberthal AS, Meissner HC, et al. Clinical Practice Guideline: The Diagnosis, Management, 288

and Prevention of Bronchiolitis. Pediatrics 2014;134:e1474–502. 289

4 Carande EJ, Pollard AJ, Drysdale SB. Management of Respiratory Syncytial Virus Bronchiolitis: 2015 290 Survey of Members of the European Society for Paediatric Infectious Diseases. Can J Infect Dis Med 291 Microbiol 2016;2016. 292

5 [Consensus conference on the management of infant bronchiolitis. Paris, France, 21 September 2000. 293 Proceedings]. Arch Pédiatrie Organe Off Sociéte Fr Pédiatrie 2001;8 Suppl 1:1s–196s. 294

6 Carsin A, Gorincour G, Bresson V, et al. La radiographie de thorax chez le nourrisson hospitalisé pour 295 bronchiolite aiguë : réelle information ou simple irradiation ? Arch Pédiatrie 2012;19:1308–15. 296

7 Arnoux V, Carsin A, Bosdure E, et al. Radiographie de thorax et bronchiolite aiguë : des indications en 297 diminution ? Arch Pédiatrie 2017;24:10–6. 298

8 Gajdos V, Katsahian S, Beydon N, et al. Effectiveness of Chest Physiotherapy in Infants Hospitalized with 299 Acute Bronchiolitis: A Multicenter, Randomized, Controlled Trial. PLOS Med 2010;7:e1000345. 300

9 Ralston S, Parikh K, Goodman D. Benchmarking Overuse of Medical Interventions for Bronchiolitis. JAMA 301 Pediatr 2015;169:805–6. 302

10 Quinonez R, Robbins E, Nazif J, et al. Decreasing unnecessary utilization in acute bronchiolitis care: 303 Results from the value in inpatient pediatrics network. J Hosp Med 2013;8. 304

11 Akenroye AT, Baskin MN, Samnaliev M, et al. Impact of a Bronchiolitis Guideline on ED Resource Use 305 and Cost: A Segmented Time-Series Analysis. Pediatrics 2014;133:e227–34. 306

12 Verstraete M, Cros P, Gouin M, et al. Prise en charge de la bronchiolite aiguë du nourrisson de moins de 307 1 an : actualisation et consensus médical au sein des hôpitaux universitaires du Grand Ouest (HUGO). Arch 308

Pédiatrie 2014;21:53–62. 309

13 Fortin N. Epidémies de bronchiolite dans l’agglomération nantaise 2007-2012. CIRE INVS de la Région 310 Pays de la Loire. 311

14 Howell V, Schwartz AE, O’Leary JD, et al. The effect of the SQUIRE (Standards of QUality Improvement 312 Reporting Excellence) guidelines on reporting standards in the quality improvement literature: a before-and-313 after study. BMJ Qual Saf 2015;24:400–6. 314

15 Florin TA, Plint AC, Zorc JJ. Viral bronchiolitis. The Lancet 2017;389:211–24. 315

16 Friedman JN, Rieder MJ, Walton JM. Bronchiolitis: Recommendations for diagnosis, monitoring and 316

management of children one to 24 months of age. Paediatr Child Health 2014;19:485–91. 317

17 Parikh K, Hall M, Teach SJ. Bronchiolitis Management Before and After the AAP Guidelines. Pediatrics 318 2014;133:e1–7. 319

18 Ralston S, Comick A, Nichols E, et al. Effectiveness of Quality Improvement in Hospitalization for 320

Bronchiolitis: A Systematic Review. Pediatrics 2014;134:571–81. 321

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19 Mittal V, Darnell C, Walsh B, et al. Inpatient Bronchiolitis Guideline Implementation and Resource 322 Utilization. Pediatrics 2014;133:e730–7. 323

20 Silver AH, Esteban-Cruciani N, Azzarone G, et al. 3% Hypertonic Saline Versus Normal Saline in Inpatient 324 Bronchiolitis: A Randomized Controlled Trial. Pediatrics 2015;136:1036–43. 325

21 Roqué i Figuls M, Giné-Garriga M, Granados Rugeles C, et al. Chest physiotherapy for acute bronchiolitis 326 in paediatric patients between 0 and 24 months old. In: Cochrane Database of Systematic Reviews. John 327 Wiley & Sons, Ltd 2016. 328

22 Schuh S, Lalani A, Allen U, et al. Evaluation of the Utility of Radiography in Acute Bronchiolitis. J Pediatr 329 2007;150:429–33. 330

23 Ecochard-Dugelay E, Beliah M, Perreaux F, et al. Clinical predictors of radiographic abnormalities among 331

infants with bronchiolitis in a paediatric emergency department. BMC Pediatr 2014;14:143. 332

24 Ecochard-Dugelay E, Beliah M, Boisson C, et al. Impact of Chest Radiography for Children with Lower 333 Respiratory Tract Infection: A Propensity Score Approach. PLOS ONE 2014;9:e96189. 334

25 Ralston SL, Garber MD, Rice-Conboy E, et al. A Multicenter Collaborative to Reduce Unnecessary Care in 335

Inpatient Bronchiolitis. Pediatrics 2016;137:1–9. doi:10.1542/peds.2015-0851 336

26 Angoulvant F, Bellêttre X, Milcent K, et al. Effect of Nebulized Hypertonic Saline Treatment in Emergency 337 Departments on the Hospitalization Rate for Acute Bronchiolitis: A Randomized Clinical Trial. JAMA 338 Pediatr 2017;:e171333–e171333. 339

27 McCulloh R, Koster M, Ralston S, et al. Use of Intermittent vs Continuous Pulse Oximetry for 340 Nonhypoxemic Infants and Young Children Hospitalized for Bronchiolitis: A Randomized Clinical Trial. 341 JAMA Pediatr 2015;169:898–904. 342

28 Cunningham S, Rodriguez A, Adams T, et al. Oxygen saturation targets in infants with bronchiolitis 343

(BIDS): a double-blind, randomised, equivalence trial. Lancet Lond Engl 2015;386:1041–8. 344

345

346

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TABLES 347


2011 n = 115 2013 n = 165 P value


Gender, male 64/115 (55.65%) 89/165 (53.94%) 0.78

History wheezing =1 12/115 (10.43%) 15/165 (9.09 %) 0.71

Comorbidity 13/115 (11.30 %) 11/165 (6.67 %) 0.17

Prematurity < 37 SA 14/115 (12.17 %) 8 /165 (4.85 %) 0.03

348

349

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350


2011 n = 115 2013 n = 165 P value



At least 1 test ᵇ 101/115 (87.83%) 52/165 (31.52) < 0.001

CXR 99/115 (86.09%) 44/165 (26.67%) < 0.001



Antibiotic use 44/115 (38.26%) 22/165 (13.33%) < 0.001





Nasogastric feed lenght, d, median (IQR) 1.5 (1.0-3.0) 2.0 (1.0-3.0) 0.698


IV hydratation length, d, median (IQR) 1.0 (1.0-1.5) 1.5 (0.5-2.0) 0.592

Oxygen use 71/115 (61.74%) 83/165 (50.30%) 0.058




% amoxicillin-clavulanic acid in ATB 28/44 (63.63%) 1/22 (4.54%) <0.001



CXR, chest -X-ray; RSV, respiratory syncytial virus; ATB, antibiotic prescription ; IV, intravenous, IQR,

interquartile range

351

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Mean cost saving per patient, €, ± SE P value

Laboratory test -26.12 ± 7.80 0.003

Imagery -17.77 ± 2.63 <0.001


Drugs -14.15 ± 12.19 0.24

Global unit functioning 40.71 ± 126.00 0.80

352

353

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FIGURE CAPTION 354


Footnotes : GP unit, general pediatric; InVs, French Institut for Public Health ; ICU, intensive care unit. 356

357

358

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195x176mm (96 x 96 DPI)

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ONLINE RESOURCE 1




2011 n = 101 2013 n = 157 P value


t east treatment 45/101 (44.55%) 43/157 (27.39%) <0.001

t east test ᵇ 90/101 (89.11%) 50/157 (31.85%) < 0.001

CXR 89/101 (88.12%) 43/157 (27.39%) < 0.001



Antibiotic use 39/101 (38.61%) 21/157 (13.38%) < 0.001






Oxygen use 66/101 (65.35%) 78/157 (49.68%) 0.013




ICU transfer 8/101 (7.92%) 7/157 (4.46%) 0.19


Treatment am n ant t s /salbutamol / corticosteroids




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ONLINE RESOURCE 2




2011 n = 102 2013 n = 154 P value

Treatment ᵃ and test ᵇ 42/102 (41.18%) 23/154 (14.94%) < 0,001

t east treatment 45/102 (41.18%) 42/154 (27.27%) < 0,001

t east test ᵇ 89/102 (87.25%) 47/154 (31,85%) < 0,001

CXR 86/102 (84.34%) 47/154 (30.52%) < 0,001

RSV Nasopharyngeal swabs 28/102 (27.45%) 22/154 (14.29%) 0,073

Inflammatory Blood test 30/102 (29.41%) 15/154 (9.74%) < 0,001

Antibiotic use 38/102 (37.25%) 22/154 (14.29%) < 0,001

Salbutamol use > 1 dose 8/102 (7.84%) 7/154 (4.55%) 0,28

Corticosteroid use 10/102 (9.80%) 5/154 (3.25%) 0,013

Chest Physiotherapy 6/102 (5.88%) 0/154 (0%) 0,009

Nasogastric fluid replacement 15/102 (14.71%) 56/154 (36.36%) < 0,001

I.V. fluid replacement 22/102 (21,59%) 19/154 (12.34%) 0,049

Oxygen use 65/102 (65,69%) 76/154 (49.35%) 0,01

O2 max, L/min, median (IQR) 0.5 (0,25-1.0) 0.5 (0,25-2.0) 0,54

Oxygen lenght, d, median (IQR) 1.5 (1.0-2.5) 1.5(1.5-3.0) 0,19

LOS in GP unit, d, median (IQR) 2.0 (1,5-3.5) 2.0 (1,5-3,5) 0,37

ICU transfer 7/102 (6.86%) 4/154 (2.60%) 0,23

All-cause 7-day readmission 4/102 (3.92%) 7/154 (4.55%) 0,59

Treatment am n ant t s /salbutamol / corticosteroids




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FRENCH PERSPECTIVE




Date Submitted by the Author: 31-Aug-2017






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TITLE PAGE 1

TITLE: 2



AUTHORS: 5











Phone : +33 2.40.08.44.54 16


The Corresponding Author has the right to grant on behalf of all authors and does grant on behalf of all authors, 18




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Lille (France). 23

ABSTRACT 24

(i) As the most recent French bronchiolitis guidelines were published in 2000, there is a current over-25



guidelines in keeping with the latest international guidelines. We hypothesize that the implementation of these 28

guidelines contributed to the quality improvement of the management of bronchiolitis in our hospital. The aim of 29

this study was to determine the impact of these guidelines on the management of bronchiolitis inpatients. 30

(ii) This retrospective before/after study design was conducted in the general pediatric unit of a tertiary care 31

French hospital, looking at one year before (i.e. the winter of 2011-2012) and one year after (i.e. the winter of 32

2013-2014) the implementation of the guidelines. Two hundred and eighty bronchiolitis inpatients, all less than 33

one year of age, were included. The primary outcome we sought to evaluate was the proportion of children 34

administered a diagnostic test associated with a treatment not routinely recommended by the guidelines. As 35

balancing measures, we evaluated the length of stay, the ICU transfer, and the readmission rates. 36

(iii) Following implementation of the guidelines, use of any given treatment associated with a diagnostic test was 37

reduced by 66% (p<0.001). There were major decreases in the use of chest X-ray (86% vs 26%, p<0.001), 38

antibiotics (38.23% vs 13.33%, p<0.001), and corticosteroids (10.43% vs 3.03%, p=0.011). Balancing measures 39

were not significantly different. 40

(iv) HUGO guidelines were effective at reducing the administration of unnecessary diagnostic tests and 41

medications. This study was the first step in convincing French pediatricians to streamline their practices until 42

updated national guidelines are published. 43

44

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What is known about the subject: 45

• Bronchiolitis results in 30.000 hospitalizations annually in France, and the most recent guidelines on the 46

subject date from 2000. 47


inpatient treatment in France. 49


• The implementation of HUGO guidelines allowed the curtailment of excessive use of chest X-rays, 51

respiratory syncytial virus testing, and inflammatory blood tests. 52

• Reducing the administration of unnecessary treatments such as corticosteroids, salbutamol, and chest 53

physiotherapy on a French population of bronchiolitis inpatients is possible. 54

55

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ABREVIATIONS 56





CXR Chest X-ray







LOS Length of stay



PCT Procalcitonin



57

58

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TEXT 59

INTRODUCTION 60

Acute viral bronchiolitis results in 30,000 hospitalizations annually in France [1]. In 2014 and 2015 the National 61

Institute for Health and Care Excellence (NICE)[2], the American Academy of Pediatrics (AAP)[3], and the 62

Canadian Pediatric Society (CPS) [4], recommended curtailing the excessive use of antibiotics, chest X-rays 63

(CXR), respiratory syncytial virus (RSV) testing, inflammatory blood test, as well as unnecessary treatments 64

such as the administration of corticosteroids, salbutamol, and chest physiotherapy. However, the most recent 65

French guidelines date from 2000 [5]. This has led to a current over-investigation and overtreatment of infants 66

hospitalized with bronchiolitis in our country. Thus, in two recent French studies[6,7], the rates of CXR, RSV 67

testing and inflammatory blood testing performed were between 59.3% and 97.8%, between 89.5% and 98.7%, 68

and around 57.7%, respectively. In the study of Arnoux et al., the rate of chest physiotherapy was observed to be 69

as high as 75% [7]. And in 2013, Gajdos et al. reported a 14% rate for salbutamol use, 10% for corticosteroids, 70

and 28% for antibiotics[8]. By comparison, Ralston et al. have proposed achievable benchmarks of cares (ABCs) 71

for inpatient care in bronchiolitis [9]: a 10-19% rate of use for bronchodilatators, a 0-9% rate of use for 72

corticosteroids, a 17-19% rate of use for antibiotics, and a 31-42% rate of use for CXR. And, in a 2010 study 73

conducted in 17 American hospitals, the rate of chest physiotherapy was 4% [10]. In addition, the rate of 74

antibiotics use and RSV testing were 10% and 29% in the study by Akenroy et al. [11]. 75


France (‘HUGO’) published guidelines in 2012 [12], that are in accord with the latest international 77

recommendations. In this study, we sought to determine the impact of these HUGO guidelines. Our primary aim 78

was to evaluate whether the streamlining of practices could be implemented in France. We hypothesized that an 79

improvement in practices, i.e., that the proportion of patients receiving treatments such as antibiotics, 80

corticosteroids, or salbutamol, and a diagnostic test such as chest X-rays, respiratory syncytial virus (RSV) 81

testing, or a blood test would be reduced following implementation of the HUGO guidelines. As secondary 82

outcomes, we evaluated the length of stay (LOS), hospitalization costs, and rates of intensive care unit (ICU) 83

transfer and readmission at seven days. We also compared the modalities of supportive care prior to and 84

following the implementation of the guidelines. 85

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METHODS 86


The Nantes University Hospital (NUH) provides pediatric care for a geographic area with a population of 88

850,000 with 12,107 births as of 2010. Each winter, bronchiolitis accounts for approximately 500 89

hospitalizations at the NUH [13]. We conducted a retrospective study of quality improvement intervention in 90

order to standardize the care provided to bronchiolitis inpatients. We compared the year prior to implementation 91

of the HUGO guidelines (i.e. the winter of 2011-2012) to the year following their implementation (i.e. the winter 92

of 2013-2014). We deemed the winter of 2012-2013 to be a transition year. 93

For each bronchiolitis season, we analyzed the three weeks of major bronchiolitis epidemics. Each year, during 94

those weeks, the NUH general pediatric unit becomes overcrowded, accommodating practically only 95

bronchiolitis inpatients. We hypothesized that the workload is similar year-over-year during those periods. 96

According to the regional office of the French Institute for Public Health of the Pays de la Loire, for the winter 97

of 2011–2012, the three major bronchiolitis epidemic weeks were weeks 48, 49, and 50. For the winter of 2013–98

2014 they were weeks 51, 52, and 1. 99


French legislation stipulates that informed consent is not required and local retrospective data may be used for an 101


This study was reported according to the SQUIRE (Standards for Quality Improvement Reporting Excellence) 103

reporting guidelines.[14]Intervention: HUGO Bronchiolitis Guidelines Development and Implementation 104

In 2011, pediatricians, pediatric pulmonologists, and emergency physicians belonging to HUGO met to analyze 105

the recent published data regarding bronchiolitis in children less than one year of age. Criteria to distinguish 106

childhood asthma from acute viral bronchiolitis were established (see online resource 1). Prescriptions of 107

diagnostic tests, antibiotics, and chest physiotherapy were defined and reserved for limited situations. Modalities 108

of oxygen supplementation and nutritional support were proposed. All these recommendations were summarized 109

in the HUGO bronchiolitis guidelines (see online resource 1)[12] . 110

The guidelines were implemented by the NUH in September 2012 by holding team meetings involving pediatric 111

nurses, physicians, and trainees. These inter-professional meetings occur annually at the start of bronchiolitis 112

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season. Daily brief meetings (just following the usual morning meeting) with physicians and nurses were also 113

organized during the 14 first days of the epidemic seasons to discuss difficulties and a summary of the guidelines 114

was posted in the emergency and the general pediatric wards. The guidelines were integrated into the NUH 115

guidelines book, and they are readily accessible online via the hospital’s intranet website. 116





and wheezing, as recommended in the HUGO and international guidelines [2–4,12]. The cut-off age of one year 121

was decided upon according to the current literature [11,15–17]. 122










Data were collected by the retrospective review of medical files in October 2014, and tabulated using Excel 132

(Microsoft, Inc, Redmond, USA). Data on the cost of services were obtained from the hospital’s administrative 133

and financial databases for each included patient. 134






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their uses are not routinely recommended by the HUGO guidelines. Moreover, they are typical outcomes used to 140








duration and the level of oxygen supplementation, as well as the duration and the type of fluid replacement. The 148

guidelines suggest limiting continuous pulse oxymetry; decreasing oxyhemoglobin saturation (SpO2) targets, 149

especially during sleep; and nasogastric feeding is preferred, with the exception of severe bronchiolitis in 150







the primary outcome, as published previously in other studies[11,19,20]. Assuming a power of 80%, α of 0.05, 157


approximately 150 bronchiolitis hospitalizations at the NUH during the three bronchiolitis epidemic weeks [13]. 159








2011). 167

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RESULTS 168




winter of 2013–2014) (Fig 1). Twenty-four children had comorbidities (see online resource 2). The 172

hospitalization rate following emergency consultation for bronchiolitis was higher in the winter of 2013–2014 173

than in the winter of 2011–2012 (p<0.001). There was no significant difference in the proportion of initial 174

hospitalizations in the ICU for bronchiolitis between the two periods (p=0.14). There were no significant 175

differences between period 1 and period 2 group characteristics, except in terms of the history of prematurity 176

<37 SA (Table 1). 177

Primary Outcome 178











In the subgroup analysis excluding patients with a history of prematurity (see online resource 3), and or those 189

with comorbidities (see online resource 4), all of the differences that were statistically significant in the general 190

outcomes analysis remained significant. The downward trends of IV and supplemental oxygen use became 191

significant. 192

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was 6.96% in the winter of 2011–2012 and 4.24% in the winter of 2013–2014 (p=0.23). The readmission rate at 198


implementation (p=0.59) (Table 2). There were no deaths during either period. 200

201

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DISCUSSION 202

MAIN RESULTS 203

This work is the first French study showing that the standardization of bronchiolitis inpatient management 204

allowed for a reduction in unnecessary testing and treatments. One year after the implementation of these 205

guidelines, we noticed significant reductions in the use of CXR, inflammatory blood tests, antibiotics, 206

corticosteroids, and chest physiotherapy, without a discernible increase in morbidity. Thus, the ABCs for 207

inpatients care in bronchiolitis proposed by Ralston et al. were reached [9]. 208

209

OVERUSE OF TESTS AND TREATMENTS IN FRANCE 210


published studies, particularly three recent studies conducted in others French university hospitals [6–8]. In the 212

study of Carsin et al. [6], the rates of nasopharyngeal viral swabs, inflammatory blood tests, and IV fluid 213

replacements were 98.7%, 57.7%, and 54%, respectively. Gajdos et al. reported a 14% rate for salbutamol use, 214

10% for corticosteroids, and 28% for antibiotics [8]. The current over-investigation and an over-treatment of 215

infants hospitalized with bronchiolitis in France is not without potential for causing harm. Chest physiotherapy 216

had no significant effect on time to recovery [21], but increased the frequency of vomiting and transitory 217

respiratory destabilization in the work of Gadjos et al.[8]. 218

219

A PRACTICE IMPROVEMENT WITHOUT DELETERIOUS EFFECTS 220

There were no significant differences between the baseline characteristics of the two periods for the populations, 221

except in terms of their history of prematurity. For this characteristic, the rate for period 1 of 12.17% was similar 222

to the finding in other studies with rates between 8.7 and 16% [6,17]. However, this difference appeared to have 223

a minor impact on our study’s outcomes. Indeed, in the subgroup analysis that excluded patients with a history of 224

prematurity, all of the statistically significant differences in the general outcomes analysis remained significant. 225

This suggests that the observed improvement is due to the implementation of the guidelines rather than the 226

changes in the typology of patients. We did not observe any significantly adverse effects of the HUGO 227

bronchiolitis guidelines on mortality, ICU transfers, or readmission rates at seven days, but this could be due to 228

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the fact that our study lacked the power to adequately evaluate this. However, previously published studies 229

involving larger populations that evaluated the impact of similar bronchiolitis guidelines did not report any 230

deleterious effects on morbidity [11,18,19]. 231

Concerning CXR, the NICE [2], the AAP [3] and the CPS bronchiolitis guidelines [4], reaffirm that 232

current evidence does not support its routine use. It should be reserved for cases of ICU admission or signs of an 233

airway complication such as pneumothorax. Indeed, the rate of differential diagnoses made thanks to CXR in 234



pre-radiography was 2.6%, and became 14.7% post-radiography [22]. Similarly, a French study showed 13.5% 237

of the children without CXR received antibiotics versus 38.8% of those with CXR [23]. And, Carsin et al. 238

reported only 3.6% of the routinely performed CXR changed bronchiolitis inpatient management [6], almost all 239

by antibiotic introduction. 240

Our results also suggest that reducing unnecessary care provided benefits in terms of LOS and was cost-241


study [19], and from 2.0 to 1.8 day in Ralston’s study [25]. In our pragmatic study, the LOS remained stable at 243

2.0 days. But it should be kept in mind that those studies excluded patients who had been transferred to the ICU 244

or who had comorbidities. Moreover, in France, a national PMSI analysis of 29,784 children hospitalized for 245

bronchiolitis showed a median LOS of 3.0 days [1]. Additionally, the mean LOS observed in the recent 246

multicentric French trial on hypertonic saline nebulization was 3.8 days [26]. Moreover, the implementation of 247

HUGO guidelines allowed for little cost savings of €54.25 per patient. By comparison, Akenroye et al. reported a 248

mean cost per patient reduced by $197 [11]. 249

In regard to supportive care, the downward trend of supplemental oxygen use that was close to 250

significance (p=0.058) can most likely be explained by the reduction of the supplemental oxygen introduction 251

limit at SpO2 < 92% (<95% if associated with signs of severity) and the promotion of intermittent pulse 252

oxymetry. Concerning intermittent pulse oxymetry monitoring, a recent randomized trial confirmed that it can be 253

routinely used in the management of bronchiolitis inpatients, who show clinical improvement[27]. The absence 254

of a decrease in the duration of oxygen supplementation in our work may be linked to the HUGO oxygen 255

discontinuation criteria (SpO2 >92% when asleep, >94% when awake). These criteria could be reassessed, 256

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particularly in light of the results of the randomized, controlled equivalence trial of Cunningham et al. that 257

revealed an SpO2 of ≥90% as being as safe and clinically effective as one of ≥94% [16]. 258

259

DETERMINANTS OF SUCCESS OF QUALITY IMPROVEMENT PROGRAM: 260

In comparison to the results of other quality improvement studies, such as those reported in Ralston’s systematic 261

review [18], we encountered better reduction rates for unnecessary diagnostic tests and treatments. This level of 262

success is probably linked to the design of our intervention, as it was a voluntary local collaborative work. A 263

large team of NUH medical staff (e.g. pediatricians, pediatric pulmonologists, and emergency physicians) were 264

involved in generating the HUGO guidelines and in their presentation in inter-professional team meetings. 265

Having a large team engagement led by a site champion is one of the major determinants of success for a 266

bronchiolitis quality improvement program, as found by Ralston et al. in their multicentric study [25]. Moreover, 267

the collaborative nature of the work helps to overcome clinical practice inertia and to promote evidence based 268

medicine [28]. 269

270

LIMITATIONS 271


we choose to evaluate the same unit during the three major bronchiolitis epidemic weeks. It may have introduced 273

bias: performance during those times may be consistently better or worse than it might be at another time. But 274

the bias was the same for the two inclusion periods. We hypothesized that the workload is similar year-over-year 275

during those busy weeks. There was no major change in the way the unit was run, senior medical staff, or nurse 276

teams between the two periods. We made the choice of a composite outcome associating treatment and 277

diagnostic test, this outcome could appear heterogeneous. Nevertheless, treatment and diagnostic testing were 278

the two main resources that tend to be misused in bronchiolitis. Having a composite outcome allowed us to 279

capture the overall impact of the HUGO guidelines. Moreover the use of each treatment and diagnostic test not 280

routinely recommended by the guidelines were evaluated separately too and we showed a clinically and 281

statistically significant reduction of most of the inadequate tests or treatments. 282

283

CONCLUSION 284

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In conclusion, we showed that reduction in the overuse of unnecessary diagnostic and therapeutic measure was 285

possible in France. Sustainability and generalizability of the observed improvement are still to be evaluated. This 286

study was a first step to convince the French pediatricians still reluctant to streamline their practices, before the 287

upcoming national French bronchiolitis guidelines. 288

289

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CONTRIBUTORS 290


collection. MB and CG performed the data analysis. MB wrote the first draft of the manuscript. All authors 292



ACKNOWLEDGMENTS 295





files. 300

FUNDING 301

No funding supported this work. 302





submitted work. 307

ETHICS APPROVAL 308





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318

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REFERENCE 319


Arch Pédiatrie 2008;15:327–8. 321




4 Friedman JN, Rieder MJ, Walton JM. Bronchiolitis: Recommendations for diagnosis, monitoring and 326 management of children one to 24 months of age. Paediatr Child Health 2014;19:485–91. 327

5 [Consensus conference on the management of infant bronchiolitis. Paris, France, 21 September 2000. 328

Proceedings]. Arch Pédiatrie Organe Off Sociéte Fr Pédiatrie 2001;8 Suppl 1:1s–196s. 329


7 Arnoux V, Carsin A, Bosdure E, et al. Radiographie de thorax et bronchiolite aiguë : des indications en 332

diminution ? Arch Pédiatrie 2017;24:10–6. 333




11 Akenroye AT, Baskin MN, Samnaliev M, et al. Impact of a Bronchiolitis Guideline on ED Resource Use 340

and Cost: A Segmented Time-Series Analysis. Pediatrics 2014;133:e227–34. 341

12 Verstraete M, Cros P, Gouin M, et al. Prise en charge de la bronchiolite aiguë du nourrisson de moins de 342 1 an : actualisation et consensus médical au sein des hôpitaux universitaires du Grand Ouest (HUGO). Arch 343 Pédiatrie 2014;21:53–62. 344


14 Ogrinc G, Davies L, Goodman D, et al. SQUIRE 2.0 (Standards for QUality Improvement Reporting 347 Excellence): revised publication guidelines from a detailed consensus process. BMJ Qual Saf 2016;25:986–348 92. 349

15 Meissner HC. Viral Bronchiolitis in Children. N Engl J Med 2016;374:62–72. doi:10.1056/NEJMra1413456 350

16 Cunningham S, Rodriguez A, Adams T, et al. Oxygen saturation targets in infants with bronchiolitis 351 (BIDS): a double-blind, randomised, equivalence trial. Lancet Lond Engl 2015;386:1041–8. 352


18 Ralston S, Comick A, Nichols E, et al. Effectiveness of Quality Improvement in Hospitalization for 355 Bronchiolitis: A Systematic Review. Pediatrics 2014;134:571–81. 356

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Inpatient Bronchiolitis. Pediatrics 2016;137:1–9. 371



28 Cabana MD, Rand CS, Powe NR, et al. Why don’t physicians follow clinical practice guidelines?: A 378

framework for improvement. JAMA 1999;282:1458–65. 379

380

381

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TABLES 382


2011 n = 115 2013 n = 165 P value


Gender, male 64/115 (55.65%) 89/165 (53.94%) 0.78

History of wheezing 12/115 (10.43%) 15/165 (9.09 %) 0.71

Comorbidity 13/115 (11.30 %) 11/165 (6.67 %) 0.17

Prematurity < 37 weeks of gestation 14/115 (12.17 %) 8 /165 (4.85 %) 0.03

SD-standard deviation 383

384

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385


2011 n = 115 2013 n = 165 P value



At least 1 test ᵇ 101/115 (87.83%) 52/165 (31.52) < 0.001

CXR 99/115 (86.09%) 44/165 (26.67%) < 0.001

RSV nasopharyngeal swabs 28/115 (24.35%) 26/165 (15.76%) 0.073

Inflammatory blood test 34/115 (29.57%) 18/165 (10.91%) < 0.001

Antibiotic use 44/115 (38.26%) 22/165 (13.33%) < 0.001





Nasogastric feed length, d, median (IQR) 1.5 (1.0-3.0) 2.0 (1.0-3.0) 0.70


IV hydration length, d, median (IQR) 1.0 (1.0-1.5) 1.5 (0.5-2.0) 0.59

Oxygen use 71/115 (61.74%) 83/165 (50.30%) 0.058


Oxygen duration, d, median (IQR) 2.0 (1.0-2.5) 2.0 (1.5-3.0) 0.10


% amoxicillin-clavulanate in ATB 28/44 (63.63%) 1/22 (4.54%) <0.001

LOS in general pediatric wards, d, median (IQR) 2.0 (1.5-3.0) 2.0 (1.5-3.0) 0.28

ICU transfer 8/115 (6.96%) 7/165 (4.2%) 0.23




CXR, chest -X-ray; RSV, respiratory syncytial virus; ATB, antibiotic prescription; IV, intravenous, IQR,

interquartile range

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386


Mean cost saving per patient, €, ± SD P value

Laboratory tests -26.12 ± 7.80 0.003

Imagery -17.77 ± 2.63 <0.001


Drugs -14.15 ± 12.19 0.24

Global unit operating costs 40.71 ± 126.00 0.80

SD- standard deviation 387

388

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22

FIGURE CAPTION 389



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195x176mm (96 x 96 DPI)

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Confidential: For Review Only

ONLINE RESOURCE 1 BENHAMIDA M, BIHOUEE T, VERSTRAETE M, GRAS LE GUEN C, LAUNAY E.

Online resource 1 Summary of HUGO guidelines for the management of bronchiolitis inpatients aged less than one year of age

Diagnosis

diagnosis and gravity assessment on the basis of history and physical examination

chest-x-ray or laboratory tests should not be performed routinely

criteria to differentiate asthma from bronchiolitis first episode of wheezing before 1 year = bronchiolitis

second episode of wheezing before 1 year with personal or familial history of atopy = a trial of salbutamol possible

if there is clinically relevant response = asthma ; if not = bronchiolitis

thirst episode of wheezing = asthma

Treatments and monitoring

not recommended bronchodilatators, corticosteroids, chest physiotherapy

target indication antibiotics only if concomitant bacterial infection (amoxicillin in acute media otitis or pneumonia)

SpO2 targets oxygen introduction limit: SpO2 < 92% (<95% if associated with signs of severity)

oxygen discontinuation criteria: SpO2 >92% when asleep, >94% when awake

limiting continuous pulse oxymetry

hydratation nasogastric feeding is preferred, with the exception of severe bronchiolitis in patients with a WANG score > 8.

SpO2 : oxyhemoglobin saturation

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ONLINE RESOURCE 2


Online Resource 2 Outcomes Pre- and Post HUGO Guideline Implementation


2011 n = 102 2013 n = 154 P value


At least 1 treatment 45/102 (41.18%) 42/154 (27.27%) < 0.001

At least 1 test ᵇ 89/102 (87.25%) 47/154 (31.85%) < 0.001

CXR 86/102 (84.34%) 47/154 (30.52%) < 0.001



Antibiotic use 38/102 (37.25%) 22/154 (14.29%) < 0.001



Chest Physiotherapy 6/102 (5.88%) 0/154 (0%) 0.009



Oxygen use 65/102 (65.69%) 76/154 (49.35%) 0.01

O2 max. L/min. median (IQR) 0.5 (0.25-1.0) 0.5 (0.25-2.0) 0.54

Oxygen lenght. d. median (IQR) 1.5 (1.0-2.5) 1.5(1.5-3.0) 0.19

LOS in GP unit. d. median (IQR) 2.0 (1.5-3.5) 2.0 (1.5-3.5) 0.37

ICU transfer 7/102 (6.86%) 4/154 (2.60%) 0.23




CXR. chest -X-ray; RSV. respiratory syncytial virus; ATB. antibiotic prescription ;

IV. intravenous; IQR. interquartile range

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ONLINE RESOURCE 3


Online Resource 3 Outcomes Pre- and Post H.U.G.O Guideline Implementation


2011 n = 101 2013 n = 157 P value


At least 1 treatment 45/101 (44.55%) 43/157 (27.39%) <0.001

At least 1 test ᵇ 90/101 (89.11%) 50/157 (31.85%) < 0.001

CXR 89/101 (88.12%) 43/157 (27.39%) < 0.001



Antibiotic use 39/101 (38.61%) 21/157 (13.38%) < 0.001





IV. fluid replacement 24/101 (23.76%) 21/157 (13.68%) 0.032

Oxygen use 66/101 (65.35%) 78/157 (49.68%) 0.013




ICU transfer 8/101 (7.92%) 7/157 (4.46%) 0.19






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nlyONLINE RESOURCE 4


Online Resource 4 Detailed comorbidities of the patients

2011 n=13 2013 n = 11

congenital heart disease 4 2

other malformation 2 2

chronic neurological disease 0 2

neonatal respiratory distress 5 3

mild bronchopulmonary dysplasia 0 1

sickle cell disease 0 1

child abuse 2 0

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FRENCH PERSPECTIVE




Date Submitted by the Author: 08-Sep-2017






jpaedsopen.bmj.com

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TITLE PAGE 1

TITLE: 2



AUTHORS: 5











Phone : +33 2.40.08.44.54 16


The Corresponding Author has the right to grant on behalf of all authors and does grant on behalf of all authors, 18




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Lille (France). 23

ABSTRACT 24

Introduction As the most recent French bronchiolitis guidelines were published in 2000, there is a current over-25



guidelines in keeping with the latest international guidelines. We hypothesize that the implementation of these 28

guidelines contributed to the quality improvement of the management of bronchiolitis in our hospital. The aim of 29

this study was to determine the impact of these guidelines on the management of bronchiolitis inpatients. 30

Methods This retrospective before/after study design was conducted in the general pediatric unit of a tertiary 31

care French hospital, looking at one year before (i.e. the winter of 2011-2012) and one year after (i.e. the winter 32

of 2013-2014) the implementation of the guidelines. Two hundred and eighty bronchiolitis inpatients, all less 33

than one year of age, hundred fifteen in 2011-12 and one hundred and sixty five in 2013-14, were included. The 34

primary outcome we sought to evaluate was the proportion of children administered a diagnostic test associated 35

with a treatment not routinely recommended by the guidelines. As balancing measures, we evaluated the length 36

of stay, the ICU transfer, and the readmission rates. 37

Results Following implementation of the guidelines, use of any given treatment associated with a diagnostic test 38

was reduced by 66% (p<0.001). There were major decreases in the use of chest X-ray (86% vs 26%, p<0.001), 39

antibiotics (38% vs 13%, p<0.001), and corticosteroids (10% vs 3%, p=0.011). Balancing measures were not 40

significantly different. 41

Conclusions HUGO guidelines were effective at reducing the administration of unnecessary diagnostic tests and 42

medications. This study was the first step in convincing French pediatricians to streamline their practices until 43

updated national guidelines are published. 44

45

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What is known about the subject: 46

• Bronchiolitis results in 30.000 hospitalizations annually in France. 47


inpatient treatment in France. 49

• The HUGO guidelines on bronchiolitis were published in 2012 50


• The implementation of HUGO guidelines allowed the curtailment of excessive use of chest X-rays, 52

respiratory syncytial virus testing, and inflammatory blood tests. 53

• Reducing the administration of unnecessary treatments such as corticosteroids, salbutamol, and chest 54

physiotherapy on a French population of bronchiolitis inpatients is possible. 55

56

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ABREVIATIONS 57





CXR Chest X-ray







LOS Length of stay



PCT Procalcitonin



58

59

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TEXT 60

INTRODUCTION 61

Acute viral bronchiolitis results in 30,000 hospitalizations annually in France [1]. In 2014 and 2015 the National 62

Institute for Health and Care Excellence (NICE)[2], the American Academy of Pediatrics (AAP)[3], and the 63

Canadian Pediatric Society (CPS) [4], recommended curtailing the excessive use of antibiotics, chest X-rays 64

(CXR), respiratory syncytial virus (RSV) testing, inflammatory blood test, as well as unnecessary treatments 65

such as the administration of corticosteroids, salbutamol, and chest physiotherapy. However, the most recent 66

French guidelines date from 2000 [5]. This has led to a current over-investigation and overtreatment of infants 67

hospitalized with bronchiolitis in our country. Thus, in two recent French studies[6,7], the rates of CXR, RSV 68

testing and inflammatory blood testing performed were between 59% and 97%, between 89% and 98%, and 69

around 57%, respectively. In the study of Arnoux et al., the rate of chest physiotherapy was observed to be as 70

high as 75% [7]. And in 2013, Gajdos et al. reported a 14% rate for salbutamol use, 10% for corticosteroids, and 71

28% for antibiotics[8]. By comparison, Ralston et al. have proposed achievable benchmarks of cares (ABCs) for 72

inpatient care in bronchiolitis [9]: a 10-19% rate of use for bronchodilatators, a 0-9% rate of use for 73

corticosteroids, a 17-19% rate of use for antibiotics, and a 31-42% rate of use for CXR. And, in a 2010 study 74

conducted in 17 American hospitals, the rate of chest physiotherapy was 4% [10]. In addition, the rate of 75

antibiotics use and RSV testing were 10% and 29% in the study by Akenroy et al. [11]. 76


France (‘HUGO’) published guidelines in 2012 [12], that are in accord with the latest international 78

recommendations. In this study, we sought to determine the impact of these HUGO guidelines. Our primary aim 79

was to evaluate whether the streamlining of practices could be implemented in France. We hypothesized that an 80

improvement in practices, i.e., that the proportion of patients receiving treatments such as antibiotics, 81

corticosteroids, or salbutamol, and a diagnostic test such as chest X-rays, respiratory syncytial virus (RSV) 82

testing, or a blood test would be reduced following implementation of the HUGO guidelines. As secondary 83

outcomes, we evaluated the length of stay (LOS), hospitalization costs, and rates of intensive care unit (ICU) 84

transfer and readmission at seven days. We also compared the modalities of supportive care prior to and 85

following the implementation of the guidelines. 86

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METHODS 87


The Nantes University Hospital (NUH) provides pediatric care for a geographic area with a population of 89

850,000 with 12,107 births as of 2010. Each winter, bronchiolitis accounts for approximately 500 90

hospitalizations at the NUH [13]. We conducted a retrospective study of quality improvement intervention in 91

order to standardize the care provided to bronchiolitis inpatients. We compared the year prior to implementation 92

of the HUGO guidelines (i.e. the winter of 2011-2012) to the year following their implementation (i.e. the winter 93

of 2013-2014). We deemed the winter of 2012-2013 to be a transition year. 94

For each bronchiolitis season, we analyzed the three weeks of major bronchiolitis epidemics. Each year, during 95

those weeks, the NUH general pediatric unit becomes overcrowded, accommodating practically only 96

bronchiolitis inpatients. We hypothesized that the workload is similar year-over-year during those periods. 97

According to the regional office of the French Institute for Public Health of the Pays de la Loire, for the winter 98

of 2011–2012, the three major bronchiolitis epidemic weeks were weeks 48, 49, and 50. For the winter of 2013–99

2014 they were weeks 51, 52, and 1. 100


French legislation stipulates that informed consent is not required and local retrospective data may be used for an 102


This study was reported according to the SQUIRE (Standards for Quality Improvement Reporting Excellence) 104

reporting guidelines.[14]Intervention: HUGO Bronchiolitis Guidelines Development and Implementation 105

In 2011, pediatricians, pediatric pulmonologists, and emergency physicians belonging to HUGO met to analyze 106

the recent published data regarding bronchiolitis in children less than one year of age. Criteria to distinguish 107

childhood asthma from acute viral bronchiolitis were established (see online resource 1). Prescriptions of 108

diagnostic tests, antibiotics, and chest physiotherapy were defined and reserved for limited situations. Modalities 109

of oxygen supplementation and nutritional support were proposed. All these recommendations were summarized 110

in the HUGO bronchiolitis guidelines (see online resource 1)[12] . 111

The guidelines were implemented by the NUH in September 2012 by holding team meetings involving pediatric 112

nurses, physicians, and trainees. These inter-professional meetings occur annually at the start of bronchiolitis 113

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season. Daily brief meetings (just following the usual morning meeting) with physicians and nurses were also 114

organized during the 14 first days of the epidemic seasons to discuss difficulties and a summary of the guidelines 115

was posted in the emergency and the general pediatric wards. The guidelines were integrated into the NUH 116

guidelines book, and they are readily accessible online via the hospital’s intranet website. 117





and wheezing, as recommended in the HUGO and international guidelines [2–4,12]. The cut-off age of one year 122

was decided upon according to the current literature [11,15–17]. 123










Data were collected by the retrospective review of medical files in October 2014, and tabulated using Excel 133

(Microsoft, Inc, Redmond, USA). Data on the cost of services were obtained from the hospital’s administrative 134

and financial databases for each included patient. 135






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their uses are not routinely recommended by the HUGO guidelines. Moreover, they are typical outcomes used to 141








duration and the level of oxygen supplementation, as well as the duration and the type of fluid replacement. The 149

guidelines suggest limiting continuous pulse oxymetry; decreasing oxyhemoglobin saturation (SpO2) targets, 150

especially during sleep; and nasogastric feeding is preferred, with the exception of severe bronchiolitis in 151







the primary outcome, as published previously in other studies [11,19,20]. Assuming a power of 80%, α of 0.05, 158


approximately 150 bronchiolitis hospitalizations at the NUH during the three bronchiolitis epidemic weeks [13]. 160








2011). 168

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RESULTS 169




winter of 2013–2014) (Fig 1). Twenty-four children had comorbidities (see online resource 2). The 173

hospitalization rate following emergency consultation for bronchiolitis was higher in the winter of 2013–2014 174

than in the winter of 2011–2012 (p<0.001). There was no significant difference in the proportion of initial 175

hospitalizations in the ICU for bronchiolitis between the two periods (p=0.14). There were no significant 176

differences between period 1 and period 2 group characteristics, except in terms of the history of prematurity 177

<37 SA (Table 1). 178

Primary Outcome 179











In the subgroup analysis excluding patients with a history of prematurity (see online resource 3), and or those 190

with comorbidities (see online resource 4), all of the differences that were statistically significant in the general 191

outcomes analysis remained significant. The downward trends of IV and supplemental oxygen use became 192

significant. 193

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was 7% in the winter of 2011–2012 and 4.2% in the winter of 2013–2014 (p=0.23). The readmission rate at 199


implementation (p=0.59) (Table 2). There were no deaths during either period. 201

202

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DISCUSSION 203

This work is the first French study showing that the standardization of bronchiolitis inpatient management 204

allowed for a reduction in unnecessary testing and treatments. One year after the implementation of these 205

guidelines, we noticed significant reductions in the use of CXR, inflammatory blood tests, antibiotics, 206

corticosteroids, and chest physiotherapy, without a discernible increase in morbidity. Thus, the ABCs for 207

inpatients care in bronchiolitis proposed by Ralston et al. were reached [9]. 208

209


published studies, particularly three recent studies conducted in others French university hospitals [6–8]. In the 211

study of Carsin et al. [6], the rates of nasopharyngeal viral swabs, inflammatory blood tests, and IV fluid 212

replacements were 98%, 57%, and 54%, respectively. Gajdos et al. reported a 14% rate for salbutamol use, 10% 213

for corticosteroids, and 28% for antibiotics [8]. The current over-investigation and an over-treatment of infants 214

hospitalized with bronchiolitis in France is not without potential for causing harm. Chest physiotherapy had no 215

significant effect on time to recovery [21], but increased the frequency of vomiting and transitory respiratory 216

destabilization in the work of Gadjos et al.[8]. 217

218

There were no significant differences between the baseline characteristics of the two periods for the populations, 219

except in terms of their history of prematurity. For this characteristic, the rate for period 1 of 12 % was similar to 220

the finding in other studies with rates between 8.7 and 16% [6,17]. However, this difference appeared to have a 221

minor impact on our study’s outcomes. Indeed, in the subgroup analysis that excluded patients with a history of 222

prematurity, all of the statistically significant differences in the general outcomes analysis remained significant. 223

This suggests that the observed improvement is due to the implementation of the guidelines rather than the 224

changes in the typology of patients. We did not observe any significantly adverse effects of the HUGO 225

bronchiolitis guidelines on mortality, ICU transfers, or readmission rates at seven days, but this could be due to 226

the fact that our study lacked the power to adequately evaluate this. However, previously published studies 227

involving larger populations that evaluated the impact of similar bronchiolitis guidelines did not report any 228

deleterious effects on morbidity [11,18,19]. 229

Concerning CXR, the NICE [2], the AAP [3] and the CPS bronchiolitis guidelines [4], reaffirm that 230

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current evidence does not support its routine use. It should be reserved for cases of ICU admission or signs of an 231

airway complication such as pneumothorax. Indeed, the rate of differential diagnoses made thanks to CXR in 232



pre-radiography was 2.6%, and became 15% post-radiography [22]. Similarly, a French study showed 14% of 235

the children without CXR received antibiotics versus 39% of those with CXR [23]. And, Carsin et al. reported 236

only 3.6% of the routinely performed CXR changed bronchiolitis inpatient management [6], almost all by 237

antibiotic introduction. 238

Our results also suggest that reducing unnecessary care provided benefits in terms of LOS and was cost-239


study [19], and from 2.0 to 1.8 day in Ralston’s study [25]. In our pragmatic study, the LOS remained stable at 241

2.0 days. But it should be kept in mind that those studies excluded patients who had been transferred to the ICU 242

or who had comorbidities. Moreover, in France, a national PMSI analysis of 29,784 children hospitalized for 243

bronchiolitis showed a median LOS of 3.0 days [1]. Additionally, the mean LOS observed in the recent 244

multicentric French trial on hypertonic saline nebulization was 3.8 days [26]. Moreover, the implementation of 245

HUGO guidelines allowed for little cost savings of €54.25 per patient. By comparison, Akenroye et al. reported a 246

mean cost per patient reduced by $197 [11]. 247

248

In regard to supportive care, the downward trend of supplemental oxygen use that was close to significance 249

(p=0.058). It could be improved by reassessing the oxygen discontinuation criteria, and promoting intermittent 250

pulse oximetry, as showed in two recent randomized trials [16, 27]. 251

252

In comparison to the results of other quality improvement studies, such as those reported in Ralston’s systematic 253

review [18], we encountered better reduction rates for unnecessary diagnostic tests and treatments. This level of 254

success is probably linked to the design of our intervention, as it was a voluntary local collaborative work. A 255

large team of NUH medical staff (e.g. pediatricians, pediatric pulmonologists, and emergency physicians) were 256

involved in generating the HUGO guidelines and in their presentation in inter-professional team meetings. 257

Having a large team engagement led by a site champion is one of the major determinants of success for a 258

bronchiolitis quality improvement program, as found by Ralston et al. in their multicentric study [25]. Moreover, 259

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the collaborative nature of the work helps to overcome clinical practice inertia and to promote evidence based 260

medicine [28]. 261

262


we choose to evaluate the same unit during the three major bronchiolitis epidemic weeks. It may have introduced 264

bias: performance during those times may be consistently better or worse than it might be at another time. But 265

the bias was the same for the two inclusion periods. We hypothesized that the workload is similar year-over-year 266

during those busy weeks. There was no major change in the way the unit was run, senior medical staff, or nurse 267

teams between the two periods. We made the choice of a composite outcome associating treatment and 268

diagnostic test, this outcome could appear heterogeneous. Nevertheless, treatment and diagnostic testing were 269

the two main resources that tend to be misused in bronchiolitis. Having a composite outcome allowed us to 270

capture the overall impact of the HUGO guidelines. Moreover the use of each treatment and diagnostic test not 271

routinely recommended by the guidelines were evaluated separately too and we showed a clinically and 272

statistically significant reduction of most of the inadequate tests or treatments. 273

274

In conclusion, we showed that reduction in the overuse of unnecessary diagnostic and therapeutic measure was 275

possible in France. Sustainability and generalizability of the observed improvement are still to be evaluated. This 276

study was a first step to convince the French pediatricians still reluctant to streamline their practices, before the 277

upcoming national French bronchiolitis guidelines. 278

279

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CONTRIBUTORS 280


collection. MB and CG performed the data analysis. MB wrote the first draft of the manuscript. All authors 282



ACKNOWLEDGMENTS 285





files. 290

FUNDING 291

No funding supported this work. 292





submitted work. 297

ETHICS APPROVAL 298





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308

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REFERENCE 309


Arch Pédiatrie 2008;15:327–8. 311




4 Friedman JN, Rieder MJ, Walton JM. Bronchiolitis: Recommendations for diagnosis, monitoring and 316 management of children one to 24 months of age. Paediatr Child Health 2014;19:485–91. 317

5 [Consensus conference on the management of infant bronchiolitis. Paris, France, 21 September 2000. 318

Proceedings]. Arch Pédiatrie Organe Off Sociéte Fr Pédiatrie 2001;8 Suppl 1:1s–196s. 319


7 Arnoux V, Carsin A, Bosdure E, et al. Radiographie de thorax et bronchiolite aiguë : des indications en 322

diminution ? Arch Pédiatrie 2017;24:10–6. 323




11 Akenroye AT, Baskin MN, Samnaliev M, et al. Impact of a Bronchiolitis Guideline on ED Resource Use 330

and Cost: A Segmented Time-Series Analysis. Pediatrics 2014;133:e227–34. 331

12 Verstraete M, Cros P, Gouin M, et al. Prise en charge de la bronchiolite aiguë du nourrisson de moins de 332 1 an : actualisation et consensus médical au sein des hôpitaux universitaires du Grand Ouest (HUGO). Arch 333 Pédiatrie 2014;21:53–62. 334


14 Ogrinc G, Davies L, Goodman D, et al. SQUIRE 2.0 (Standards for QUality Improvement Reporting 337 Excellence): revised publication guidelines from a detailed consensus process. BMJ Qual Saf 2016;25:986–338 92. 339

15 Meissner HC. Viral Bronchiolitis in Children. N Engl J Med 2016;374:62–72. doi:10.1056/NEJMra1413456 340

16 Cunningham S, Rodriguez A, Adams T, et al. Oxygen saturation targets in infants with bronchiolitis 341 (BIDS): a double-blind, randomised, equivalence trial. Lancet Lond Engl 2015;386:1041–8. 342


18 Ralston S, Comick A, Nichols E, et al. Effectiveness of Quality Improvement in Hospitalization for 345 Bronchiolitis: A Systematic Review. Pediatrics 2014;134:571–81. 346

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Inpatient Bronchiolitis. Pediatrics 2016;137:1–9. 361



28 Cabana MD, Rand CS, Powe NR, et al. Why don’t physicians follow clinical practice guidelines?: A 368

framework for improvement. JAMA 1999;282:1458–65. 369

370

371

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TABLES 372


2011 n = 115 2013 n = 165 P value


Gender, male 64/115 (56%) 89/165 (54%) 0.78

History of wheezing 12/115 (10%) 15/165 (9.1 %) 0.71

Comorbidity 13/115 (11%) 11/165 (6.7 %) 0.17

Prematurity < 37 weeks of gestation 14/115 (12%) 8 /165 (4.9 %) 0.03

SD-standard deviation 373

374

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375


2011 n = 115 2013 n = 165 P value

Treatmentᵃ and test ᵇ 52/115 (45%) 25/165 (15%) < 0.001

At least 1 treatment 52/115 (45%) 46/165 (28%) 0.003

At least 1 test ᵇ 101/115 (88%) 52/165 (32%) < 0.001

CXR 99/115 (86%) 44/165 (27%) < 0.001

RSV nasopharyngeal swabs 28/115 (24%) 26/165 (16%) 0.073

Inflammatory blood test 34/115 (30%) 18/165 (11%) < 0.001

Antibiotic use 44/115 (38%) 22/165 (13%) < 0.001


Corticosteroid use 12/115 (10%) 5/165 (3.0%) 0.011


Nasogastric fluid replacement 19/115 (17%) 58/165 (35%) < 0.001

Nasogastric feed length, d, median (IQR) 1.5 (1.0-3.0) 2.0 (1.0-3.0) 0.70

IV fluid replacement 25/115 (22%) 22/165 (13%) 0.064

IV hydration length, d, median (IQR) 1.0 (1.0-1.5) 1.5 (0.5-2.0) 0.59

Oxygen use 71/115 (62%) 83/165 (50%) 0.058


Oxygen duration, d, median (IQR) 2.0 (1.0-2.5) 2.0 (1.5-3.0) 0.10

% amoxicillin in ATB 9/44 (20%) 19/22 (86%) <0.001

% amoxicillin-clavulanate in ATB 28/44 (64%) 1/22 (4.5%) <0.001

LOS in general pediatric wards, d, median (IQR) 2.0 (1.5-3.0) 2.0 (1.5-3.0) 0.28

ICU transfer 8/115 (7%) 7/165 (4.2%) 0.23




CXR, chest -X-ray; RSV, respiratory syncytial virus; ATB, antibiotic prescription; IV, intravenous, IQR,

interquartile range

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376


Mean cost saving per patient, €, ± SD P value

Laboratory tests -26.12 ± 7.80 0.003

Imagery -17.77 ± 2.63 <0.001


Drugs -14.15 ± 12.19 0.24

Global unit operating costs 40.71 ± 126.00 0.80

SD- standard deviation 377

378

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FIGURE CAPTION 379



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195x176mm (96 x 96 DPI)

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Confidential: For Review Only

ONLINE RESOURCE 1 BENHAMIDA M, BIHOUEE T, VERSTRAETE M, GRAS LE GUEN C, LAUNAY E.

Online resource 1 Summary of HUGO guidelines for the management of bronchiolitis inpatients aged less than one year of age

Diagnosis

diagnosis and gravity assessment on the basis of history and physical examination

chest-x-ray or laboratory tests should not be performed routinely

criteria to differentiate asthma from bronchiolitis first episode of wheezing before 1 year = bronchiolitis

second episode of wheezing before 1 year with personal or familial history of atopy = a trial of salbutamol possible

if there is clinically relevant response = asthma ; if not = bronchiolitis

thirst episode of wheezing = asthma

Treatments and monitoring

not recommended bronchodilatators, corticosteroids, chest physiotherapy

target indication antibiotics only if concomitant bacterial infection (amoxicillin in acute media otitis or pneumonia)

SpO2 targets oxygen introduction limit: SpO2 < 92% (<95% if associated with signs of severity)

oxygen discontinuation criteria: SpO2 >92% when asleep, >94% when awake

limiting continuous pulse oxymetry

hydratation nasogastric feeding is preferred, with the exception of severe bronchiolitis in patients with a WANG score > 8.

SpO2 : oxyhemoglobin saturation

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ONLINE RESOURCE 2




2011 n = 102 2013 n = 154 P value

Treatment ᵃ and test b 42/102 (41%) 23/154 (15%) < 0.001

At least 1 treatment 45/102 (41%) 42/154 (27%) < 0.001

At least 1 test b 89/102 (87%) 47/154 (32%) < 0.001

CXR 86/102 (84%) 47/154 (31%) < 0.001

RSV Nasopharyngeal swabs 28/102 (27%) 22/154 (14%) 0.073

Inflammatory Blood test 30/102 (29%) 15/154 (9.7%) < 0.001

Antibiotic use 38/102 (37%) 22/154 (14%) < 0.001




Nasogastric fluid replacement 15/102 (15%) 56/154 (36%) < 0.001

I.V. fluid replacement 22/102 (22%) 19/154 (12%) 0.049

Oxygen use 65/102 (66%) 76/154 (49%) 0.01




ICU transfer 7/102 (6.9%) 4/154 (2.6%) 0.23






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ONLINE RESOURCE 3




2011 n = 102 2013 n = 154 P value

Treatment ᵃ and test b 42/102 (41%) 23/154 (15%) < 0.001

At least 1 treatment 45/102 (41%) 42/154 (27%) < 0.001

At least 1 test b 89/102 (87%) 47/154 (32%) < 0.001

CXR 86/102 (84%) 47/154 (31%) < 0.001

RSV Nasopharyngeal swabs 28/102 (27%) 22/154 (14%) 0.073

Inflammatory Blood test 30/102 (29%) 15/154 (9.7%) < 0.001

Antibiotic use 38/102 (37%) 22/154 (14%) < 0.001




Nasogastric fluid replacement 15/102 (14 %) 56/154 (36%) < 0.001

I.V. fluid replacement 22/102 (21%) 19/154 (12%) 0.049

Oxygen use 65/102 (65%) 76/154 (49%) 0.01




ICU transfer 7/102 (6.9%) 4/154 (2.6%) 0.23






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nlyONLINE RESOURCE 4


Online Resource 4 Detailed comorbidities of the patients

2011 n=13 2013 n = 11

congenital heart disease 4 2

other malformation 2 2

chronic neurological disease 0 2

neonatal respiratory distress 5 3

mild bronchopulmonary dysplasia 0 1

sickle cell disease 0 1

child abuse 2 0

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bmj paediatrics open is committed to open peer review. as part … · 80 paediatric infectious...

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