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Original article

Chest auscultatory signs in infants presenting to A&E with bronchiolitis Kirsty E. McLellana, Ju¨rgen Schwarzea and Tom Beattiea,b Background Anecdotally it has been noted that the traditional chest signs associated with bronchiolitis appear inconsistently in infants clinically diagnosed with bronchiolitis. We wished to explore this more formally. Objective The aim of this study was to assess whether the auscultatory chest signs at presentation in infants with bronchiolitis were influenced by age or by the underlying pathogen. Materials and methods We conducted a prospective opportunistic cohort study, recruiting infants less than 12 months old who presented with bronchiolitis to the Emergency Department of the Royal Hospital for Sick Children in Edinburgh. Results Eighty-six infants were recruited. Infants who presented with wheeze were significantly older [26.6 (±1.9) weeks] than those without wheeze [17.3 (±2.1) weeks] (analysis of variance, P = 0.002). Those who presented without any chest signs on auscultation were younger than those with chest signs [15.1 (±2.6) weeks compared with 24.4 (±1.7) weeks] (analysis of variance, P = 0.006). We did

Introduction Bronchiolitis is a viral respiratory tract infection, which affects children below 12 months old and typically presents with coryzal symptoms, cough and increased respiratory effort. Clinical signs include wheeze and crackles on auscultation, fever, tachycardia, tachypnoea and increased work of breathing [1]. Occurring in the winter months (usually October to February in the UK), bronchiolitis is the leading cause of admission (7–9% of paediatric hospital admissions [2]) during this time. The hospitalization rate for bronchiolitis is 31.2 per 1000 every year [3] for children less than 12 months old. The mortality rate of bronchiolitis is low at 0.002% [4] but rises in those with underlying congenital heart disease or lung disorders (cystic fibrosis and bronchopulmonary dysplasia [5,6]). This predictable annual epidemic presents a significant burden on healthcare services as well as significant morbidity and some mortality among young infants. The majority of cases are caused by respiratory syncytial virus (RSV) (70%) [7]. Other viruses reported in bronchiolitis include influenza A/B, parainfluenza, rhinovirus, adenovirus, coronaviruses [8] and human metapneumovirus [9]. RSV infections are common; however, while 95% of infants are infected by RSV by their second winter, only 22% of infants develop significant disease [10] c 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins 0969-9546

not detect any difference in any of the auscultatory chest signs (crackles, wheeze or absence of signs) depending on the virus responsible for bronchiolitis. Conclusion Clinical signs associated with bronchiolitis vary according to age. Infants older than 6 months are more likely to present with wheeze and infants less than 4 months old are likely to present without chest signs on auscultation. European Journal of Emergency Medicine c 2014 Wolters Kluwer Health | Lippincott 21:436–441 Williams & Wilkins. European Journal of Emergency Medicine 2014, 21:436–441 Keywords: auscultation, bronchiolitis, chest signs, infants, wheeze a Department of Child Life and Health, University of Edinburgh and bRoyal Hospital for Sick Children, Edinburgh, UK

Correspondence to Tom Beattie, MBChB, MSc, FRCSEd(A&E), FCEM, FRCPE, FFSEM, DCH, Royal Hospital for Sick Children, 9 Sciennes Road, Edinburgh, Midlothian EH91LF, UK Tel: + 44 131 536 0000; fax: + 44 131 536 0052; e-mail: [email protected] Received 22 September 2013 Accepted 11 December 2013

and more research is needed to determine whether viral bronchiolitis contributes to asthma development [11,12]. Despite extensive research into bronchiolitis, treatment remains largely supportive, including nasal suction, oxygen, nasogastric feeding and ventilation for severely ill infants [13]. There is controversy surrounding the role of some potential treatments for bronchiolitis. Terbutaline [14], montelukast [15] and ipratropium bromide [16,17] have been proven ineffective. Ribavirin is not required for otherwise healthy children [18] and studies have failed to show definite benefit from ribavirin [4]. Prophylactic palivizumab (a monoclonal antibody) is not routinely utilized in clinical practice [19–21], although it may be beneficial in high-risk infants [22]. The role of corticosteroids is controversial, some studies show there is an effect [8] and that it may reduce recurrent wheeze, which follows 30% of RSV + bronchiolitis [23]; however, recent trials have shown that steroids are not effective [18,24]. However, the role of bronchodilators remains controversial [7,16]. A recent Cochrane review concluded that bronchodilators did not reduce the rate or duration of hospitalization [25] but there is a small improvement in clinical scores and some studies clearly show a positive response to bronchodilators [26,27]. It is known that auscultation signs in bronchiolitis include wheeze, crackles, DOI: 10.1097/MEJ.0000000000000115

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Chest auscultatory signs in bronchiolitis Mclellan et al. 437

as well as generalized decreased breath sounds secondary to pulmonary hyperinflation and trapping of air [4]. However, little work has been done looking specifically at chest signs on auscultation in bronchiolitis and at factors leading to different auscultatory signs. Given that the effect of treatment may be related to underlying pathology and clinical chest signs we believe that the improved recognition of the factors related to individual chest signs may contribute to improving the management of bronchiolitis. We therefore tested the hypotheses that:

Results

(1) Chest signs are related to age and that older infants present with wheeze, whereas younger infants are more likely to present with crackles. (2) Chest signs are related to the virus responsible for bronchiolitis, with different viruses causing different chest signs.

Characteristics of infants admitted to the hospital with bronchiolitis

Materials and methods We conducted a prospective opportunistic study of the infants with bronchiolitis, which was approved by the Regional Ethics Committee. Written consent was obtained from a parent or guardian of each patient. Infants who presented to the Emergency Department (ED) of the Royal Hospital for Sick Children, Edinburgh with bronchiolitis between 25 October and 23 December 2011 were recruited if they fulfilled the inclusion criteria: a clinical diagnosis of bronchiolitis (established by the senior ED doctor) and age below 12 months. The clinical picture used to diagnose bronchiolitis was that of an infant presenting with respiratory distress associated with a coryzal prodrome and associated signs of tachypnoea, tachycardia, inspiratory intercostal/sternal recession and/or hyperexpanded lungs (liver edge palpable below ribcage). We used a proforma to record clinical examination findings from the infants, specifically signs of respiratory distress (nasal flaring, head bobbing, tracheal tug, intercostal, sub costal and sternal recessions), findings of chest auscultation (crackles, wheeze) and history of apnoeas. Patient’s observations, management, inpatient care and outcome were recorded from the clinical records. Nasopharyngeal aspiration was undertaken in infants who were admitted for bronchiolitis and those who had copious secretions, according to the hospital protocol. Virology PCR results were obtained from patient records when available, usually after hospital discharge. Relevant data from the proformas were recorded in an Excel database (Microsoft 2007; Microsoft Corporation, Redmond, Washington, USA). Minitab 15 (Minitab Inc., State College, Pennsylvania, USA) was used for statistical analysis. Pearson’s w2-tests and one-way analysis of variance (ANOVA) tests were used as appropriate. P values of 0.005 or less were regarded as statistically significant.

Descriptive analysis

Eighty-six infants were recruited into the study. Their mean (±SE) age was 22.0 (±1.5) weeks and ranged from 2 to 48 weeks. Test of normality (Ryan–Joiner test) was performed and confirmed that the distribution of age was consistent with normal distribution (RJ = 0.976, P < 0.01). Sixty per cent (n = 52) of the infants recruited to this study were males.

Thirty-four (40%) infants recruited with bronchiolitis were admitted to the hospital. Eighteen (53%) (n = 18) females were admitted [ward or high-dependency unit (HDU)] compared with 16 (31%) males (w2, d.f. = 1, P = 0.04). Furthermore, two (6%) females and one (2%) male were admitted to HDU. Infants who were admitted (ward or HDU) were significantly younger than those who were discharged; the mean (±SE) age of infants who were admitted was 15.4 (±2.3) weeks, whereas that of infants who were discharged was 26.3 (±1.8) weeks (ANOVA, P = 0.0005). Furthermore, infants who were admitted to HDU were significantly younger [8.3 (±1.9) weeks] than those who were admitted to the ward [16.0 (±2.4) weeks] and those who were discharged [26.3 (±1.8) weeks] (ANOVA, P = 0.001). Chest signs in infants with bronchiolitis

During recruitment of infants it was observed that in addition to the anticipated subgroups of children who presented with wheeze, crackles and both wheeze and crackles, there was a fourth group of infants who had no added auscultatory chest signs. This subgroup included children with both normal and reduced breath sounds. Forty-three (50.0%) infants presented with wheeze, 48 (55.8%) had crackles, 27 (31.4%) had both wheeze and crackles and 22 (25.6%) had neither wheeze nor crackles. The mean age of infants according to chest signs is shown in Fig. 1a. There was a statistically significant difference in the mean (±SE) age of the infants who presented with wheeze [26.3 (±3.3) weeks], crackles [19.7 (±3.4) weeks], both wheeze and crackles [26.8 (±2.3) weeks] and no chest signs [15.1 (±2.6) weeks] (Fig. 1a). Children with wheeze were older, 26.6 (±1.9) weeks, than those infants without wheeze, 17.3 (±2.1) weeks (ANOVA, P = 0.002) (Fig. 1b). There was no statistical difference in age of infants who present with [23.7 (±2.0)] or without [19.8 (±2.2)] crackles (ANOVA, P = 0.195).

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European Journal of Emergency Medicine 2014, Vol 21 No 6

Fig. 1

(a)

(b)

35

30

∗∗

30

∗∗∗

25

Age (Weeks)

25 20 20 15

15

10

10

5

5 0 Wheeze

Crackles Wheeze+crackles

0

Neither

Yes

No

Chest signs

Wheeze

(c) ∗∗∗

25

Age (Weeks)

20 15 10 5 0 Yes

No Signs

(a) Age difference according to chest signs (mean±SE) [one-way analysis of variance (ANOVA), **P = 0.01]. (b) Age of infants according to the presence and absence of wheeze (mean±SE) (one-way ANOVA, ***P = 0.002). (c) The age of infants who present with or without chest signs (mean±SE) (one-way ANOVA, ***P = 0.006).

Children who present without any chest signs on auscultation were significantly younger at 15.1 (±2.6) weeks than those who had chest signs at 24.4 (±1.7) weeks (ANOVA, P = 0.006) (Fig. 1c). Although there was no statistically significant difference in the presence of wheeze or crackles according to sex, there seemed to be a trend with more males with wheeze and crackles compared with females. There was a statistically significant difference in the presence or absence of chest signs according to sex with more females without chest signs than males (Table 1). However, the mean age of female infants was 19.5 (±2.3) weeks compared with 23.6 (±1.9) weeks for male infants, so the higher incidence of absence of auscultatory chest signs in female infants may be a reflection of the younger age of female infants compared with males.

Apnoea

Eight infants had apnoeic episodes (mean age 7.8 weeks). Of those, four (50%) had no clinical signs on auscultation, whereas only 23% (n = 18) of infants without apnoeic episodes had no clinical signs. This is not statistically

Percentage of males and females who present with wheeze, crackles or no auscultatory chest signs

Table 1

Signs Wheezea Cracklesa None

Male [n (%)]

Female [n (%)]

P value (ANOVA)

30 (57.7) 32 (61.5) 8 (15.4)

13 (38.2) 16 (47.1) 14 (41)

0.078 0.186 0.007

ANOVA, analysis of variance. a Some infants presented with both wheeze and crackles.

significant (w2, d.f. = 1, P = 0.09) but the numbers are small. Chest signs and viruses detected in bronchiolitis

Fifty infants (58%) had upper airway suction and virology samples of nasopharyngeal aspirate (only admitted infants and those with copious secretions). The prevalence of viral pathogens identified is shown in Table 2. There were no significant differences in chest signs between different viruses detected (RSV, rhinovirus or adenovirus) or in the presence of multiple viruses. The number of infants with viruses isolated on nasopharyngeal aspirate with and without auscultatory chest signs is shown in Table 3.

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Chest auscultatory signs in bronchiolitis Mclellan et al.

Virology results from nasopharyngeal aspirates taken from 50 infants

Table 2

Viruses

Number of infants in whom virus isolated [n (%)]

RSV Rhinovirus Adenovirus RSV + another virus Multiple viruses

34 16 5 11 15

(68) (32) (10) (22) (30)

RSV, respiratory syncytial virus.

Table 3 Percentage positive virology with and without auscultatory chest signs Virology results RSV Rhinovirus Adenovirus

Chest signs [n (%)]

No auscultatory chest signs [n (%)]

24 (71) 11 (69) 3 (60)

10 (29) 5 (31) 2 (40)

Results are nonsignificant. RSV, respiratory syncytial virus.

Discussion Bronchiolitis is a common disease, accounting for a significant proportion of hospital admissions, morbidity and mortality of young children during the winter months. This is the first study, to our knowledge, which focuses on the auscultatory chest signs in infants with bronchiolitis. We anticipated that three subgroups of infants would present with wheeze, crackles or wheeze and crackles but it was unexpected that a fourth group of infants was identifiable without chest signs on auscultation. This is the first study, to our knowledge, to demonstrate these infants, who were clinically unwell, with respiratory distress, tachycardia, tachypnoea, but no signs on auscultation. Children who presented with wheeze were significantly older than infants who presented with crackles or no signs. The youngest cohort of infants were those who presented without auscultatory chest signs. This is the first time that it has been shown that auscultatory chest signs in bronchiolitis are related to the age of the infant. The finding that infants can be classified into groups according to their signs on auscultation might have implications for the management of their bronchiolitis. One of the major controversies in bronchiolitis surrounds the role of therapeutic management, specifically b-agonist therapy. Some studies have shown that bronchodilators may be beneficial [26] and the pathophysiology of RSV bronchiolitis (airway narrowing, smooth muscle contraction and oedema) suggests that patients would be likely to respond. In practice, it seems that some patients respond, whereas others do not and so far it is unknown why this is the case [8]. Clinical signs that bronchiolitis causes could determine management as infants who present with wheeze only or predominantly might respond to b-agonist. We suggest that the reason for controversy surrounding the merits of b-agonists is

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that some studies may have included patients with bronchiolitis who rather than presenting with wheeze, may have crackles or possibly even no chest signs. We postulate that infants older than 6 months with wheeze are more likely to respond to bronchodilators and suggest that future research on bronchiolitis should stratify infants by chest signs and age. Research focussing on the role of bronchodilators in the subgroup with wheeze would finally confirm or reject the role of bronchodilators in bronchiolitis. Such an approach has been suggested by Issacs [7] who recommended that ‘when wheeze predominates, a trial of nebulized b-agonist is indicated’ and has already been used in studies [28]. Perhaps in the future bronchiolitis should be redefined as bronchiolitis with and bronchiolitis without wheeze if benefit from bronchodilators is established in those with wheeze. Inhalation therapy, using racemic adrenaline, has shown no improvement in clinical results compared with inhaled saline [29]. This study should perhaps be repeated focussing on infants with predominant wheeze. Some suggest that crackles are the consistent sign in bronchiolitis and children who present with wheeze are more likely to develop asthma [7]. A recent study showed that significant risk factors for the development of asthma were previous wheezing episode secondary to rhinovirus (the strongest risk factor), RSV or other respiratory pathogen during infancy [30]. Our study has shown that crackles are a less consistent feature than previously thought, affecting just over half of bronchiolitis cases. Our study has shown that infants can present with wheeze, crackles or neither. These infants all have signs of respiratory distress, tachycardia, tachypnoea and testing has confirmed viral pathogens. We are aware that the assessment of severity of bronchiolitis cannot only be based on auscultatory signs, as we have stated absence of wheeze and hypoventilation can represent a subset of infants with high clinical severity. We also aimed to assess whether chest signs were determined by the causative virus. In our study 68% of infants with bronchiolitis had RSV, as reported by Marguet et al. [31]. Thirty per cent in our series had multiple viruses and 32% had rhinovirus, both consistent with previous reports [32,33]. Twenty-two per cent of our cohort of RSV + infants were co-infected with other viruses, similar to previous reports (24%) [34]. We did not find a correlation between chest signs and viral pathogen, but our study was not sufficiently powered to exclude an association. However, our results suggest that the clinical signs in bronchiolitis are not determined by the virus but rather the child’s response to the virus. It has been suggested that bronchiolitis should be reclassified according to the responsible virus [35]; however, this study indicates that the response of the host is determined by the child’s age and thus possibly by lung development or developing antiviral immune and inflammatory responses during the first year of life. Furthermore, our findings that

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440 European Journal of Emergency Medicine 2014, Vol 21 No 6

older infants present with wheeze leads to the possibility that these infants are on the spectrum of viral-induced wheeze and may even go on to develop asthma. It has been suggested that there is a link between bronchiolitis in infancy and asthma in childhood. One study by Sigurs et al. [23] showed that RSV resulting in hospitalization is associated with increased atopy and asthma in childhood; however, this has not been supported by other studies. Rhinovirus has been implicated as a bronchiolitis pathogen that may lead to asthma [36] and more research is needed to determine whether RSV predisposes to asthma, if children susceptible to asthma are predisposed to more severe bronchiolitis, if the latter is a promoting factor in asthma development, or if there is, in fact, no link between bronchiolitis and asthma. There are conflicting reports in the literature that different viruses lead to different disease severity, some but not others suggesting that rhinovirus [33], RSV [31] or multiple viruses [31,32] cause more severe disease. In addition to such conflicting reports, our findings that different viruses (RSV, rhinovirus, adenovirus or multiple viruses) do not cause different auscultatory chest signs, provide further support for the concept that it is the host response that determines clinical signs and severity of bronchiolitis instead of the individual virus. An important implication from this study is for general practitioners and ED doctors who need to be aware that the absence of chest signs, with increased work of breathing, tachycardia and tachypnoea does not preclude the diagnosis of bronchiolitis. In fact, doctors should be most vigilant with infants with bronchiolitis but without auscultation chest signs as they are likely to be younger and more unwell (all the infants admitted to HDU with bronchiolitis had no chest signs). There are a number of limitations to this study. First, the number of patients enrolled was not as high as anticipated, largely because of the later than expected start to the bronchiolitis season compared with previous years. Our study is not adequately powered to definitively state at which ages signs will appear, but the trends shown by this study are clear and we think the finding that younger infants are less likely to have chest signs has crucial implications on patient care. Second, our sample was a convenience sample, and although we recruited the majority of patients, it was not possible to recruit every patient. We did not take into account corrected ages for premature infants, using instead actual ages and these infants may be at a different stage of lung development than their corrected age. Conclusion

This research adds to the knowledge of bronchiolitis with the important finding that infants less than 4 months old are unlikely to present with wheeze or crackles and that clear chests (with absence of wheeze or crackles) in

younger infants with bronchiolitis should raise concern. On the contrary, infants older than 6 months are more likely to present with wheeze, and therefore we postulate that more research needs to be done to finally determine whether this subset of infants might benefit from b-agonist treatment.

Acknowledgements The authors acknowledge the help provided by the staff at the ED at RHSCE and the parents and children who participated. Conflicts of interest

There are no conflicts of interest.

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Chest auscultatory signs in infants presenting to A&E with bronchiolitis.

Anecdotally it has been noted that the traditional chest signs associated with bronchiolitis appear inconsistently in infants clinically diagnosed wit...
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