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Pediatric Pulmonology

Severity Scoring Systems: Are They Internally Valid,


Reliable and Predictive of Oxygen Use in Children With
Acute Bronchiolitis?
Gabrielle B. McCallum, MPH,1* Peter S. Morris, PhD,1,2 Clare C. Wilson, MPH,1
Lesley A. Versteegh, ENurs,1 Linda M. Ward, M. Med. Sci.(Clin.Epi),1
Mark D. Chatfield, MA, Msc,1 and Anne B. Chang, PhD1,3,4
Summary. Background: Severity scores are commonly used in research and clinically to as-
sess the severity of bronchiolitis. However, there are limitations as few have been validated.
The aim of our study was to: (i) determine the validity and reliability of a bronchiolitis scoring
system, and (ii) examine if the score predicted the need for oxygen at 12 and 24 hrs. Children
aged <24 months presenting to Royal Darwin Hospital with a clinical diagnosis of bronchiolitis
were eligible to participate. Study Design: We reviewed published papers that used a bronchi-
olitis score and summarized the data in a table. We chose the Tal score that was easy to use
and encompassed clinically important parameters. Three research nurses, trained to assess
children, used two scoring systems (Tal and Modified-Tal; respiratory rate, accessory muscle
use, wheezing, cyanosis, and oxygen saturation), blindly evaluated children within 15 min of
each other. Results: The children’s (n ¼ 115) median age was 5.4 months (IQR 2.9, 10.4);
65% were male and 64% were Indigenous. Internal consistency was excellent (Tal: Cronbach
a ¼ 0.66; Modified-Tal: a ¼ 0.70). There was substantial inter-rater agreement; weighted kap-
pa of 0.72 (95% CI: 0.63, 0.83) for Tal and 0.70 (95% CI: 0.63, 0.76) for Modified-Tal. For
predicting requirement for oxygen at 12 and 24 hrs; area under receiver operating curve
(aROC) was 0.69 (95% CI: 0.13, 1.0) and 0.75 (95% CI: 0.34, 1.0), respectively. Conclusion:
The Tal and Modified-Tal scoring systems for bronchiolitis is repeatable and can reliably be
used in research and clinical practice. Its utility for prediction of O2 requirement is limited.
Pediatr Pulmonol. ß 2012 Wiley Periodicals, Inc.

Key words: bronchiolitis severity scoring; respiratory distress assessment instrument;


RDAI.

Funding source: NHMRC, Numbers: 605809, 545216.

INTRODUCTION criteria for hospitalization of a child with bronchiolitis


are the need for oxygen or fluid management. Like
Worldwide, bronchiolitis is the most common severe Alaskan Native infants,2 Indigenous Northern Territory
acute lower respiratory tract infection.1 The usual (NT) infants have very high hospitalization rates of

1
Child Health Division, Menzies School of Health Research, Charles G.M. set up and coordinated the study, performed the data analysis and
Darwin University, Darwin, Northern Territory, Australia. drafted the manuscript. A.C. conceptualized the study, interpreted the data
and edited the manuscript. P.M. assisted in data interpretation and contrib-
2
Department of Paediatrics, Royal Darwin Hospital, Darwin, Northern uted to the manuscript. M.C. and L.W. assisted in the data analysis and
Territory, Australia. edited the manuscript. L.V. and C.W. participated in recruiting participants
and edited the manuscript. All authors read and approved the manuscript.
3
Queensland Children’s Respiratory Centre, Royal Children’s Hospital,
Brisbane, Queensland, Australia. *Correspondence to: Gabrielle B. McCallum, MPH, Menzies School of
Health Research, PO Box 41096, Casuarina, Darwin, NT 0811, Australia.
4
Queensland Children’s Respiratory Centre, Queensland’s Medical Re- E-mail: gabrielle.mccallum@menzies.edu.au
search Institute, Royal Children’s Hospital, Brisbane, Queensland, Australia.
Received 30 April 2012; Accepted 30 May 2012.
The authors declare that they have no financial competing interests.
DOI 10.1002/ppul.22627
The results of this study were presented as a poster at the Thoracic Published online in Wiley Online Library
Society of Australia and New Zealand (TSANZ) in Canberra, Australia (wileyonlinelibrary.com).
(April 2012).

ß 2012 Wiley Periodicals, Inc.


2 McCallum et al.

bronchiolitis (352 per 1,000) and the majority are phases at ‘‘segmental lobes’’ is unlikely to be repeat-
retrieved from remote communities.3 In these settings, able outside of a specialist setting. The validation of
there are often no resident medical practitioners and various scoring systems8 (see Table 1) only looked at
nurses are the acute care providers. Availability of a inter-rater agreement (some between doctors only). To
scoring system for bronchiolitis that is valid when date, none of the scoring systems has been used to pre-
used by different providers, as suggested by Liu et al.4 dict oxygen requirement; examined the other compo-
would be beneficial as acute assessment of the nents of validation of a scale to the level described by
severity of bronchiolitis will contribute to good clinical Ducharme et al.11 for asthma; or been applied to differ-
management. ent populations and settings. Indeed, the lack of reliable
Standardization of severity scoring is also important clinical tools to evaluate disease severity in clinical
for clinical research purposes. A number of clinical practice is evident. Measurement of infant lung function
scoring systems, some with modifications, have been is limited to research laboratories.
used in the many research studies on bronchiolitis5 The aim of this study was to determine if a bronchi-
(Table 1). Despite their widespread use, many of these olitis scoring system (Tal et al.8 and its modification)
scoring systems have limited validity when systemati- undertaken by trained nurses is valid (inter-rater reli-
cally evaluated and often were modified to suit individ- ability and internal consistency) and a useful predictor
ual research outcomes (Table 1 and table in Gajdos of disease severity (need for supplementary oxygen at
et al5). These scoring systems have different levels of 12 and 24 hr post assessment).
complexity (such as auscultation in ‘‘segmental lobes’’
and distinction of wheeze through parts of inspiratory METHODS
and expiratory phases), clinical parameters (e.g. the
widely used Lowell score6 does not take into account Study Design
SpO2 or cyanosis) and varying degrees of validation A prospective cohort study of children presenting to
(many were not validated), thus making it difficult to Royal Darwin Hospital (RDH) with a clinical diagnosis
evaluate across clinical research studies. Not surprising- of bronchiolitis were recruited from October 2010 to
ly, the Scottish Intercollegiate Guidelines Network December 2011. Informed consent was obtained from
(SIGN) bronchiolitis guideline stated ‘‘No good quality parents or legal guardians and the study was approved
evidence on the use of formal clinical scoring systems by our institution’s Human Research Ethics Committee.
in infants with acute bronchiolitis was identified.’’7 Three study nurses visited the paediatric ward and
Gadjos et al.5 reviewed available bronchiolitis scor- emergency department twice daily to assess eligible
ing systems and validated a system that encompassed children. Children were eligible to be enrolled if they
three parameters (respiratory rate (RR), wheeze, and were aged <24 months and presented to RDH where a
retractions). However their validation, like many other clinical diagnosis of bronchiolitis was made by the
scoring systems, consisted only of inter-rater agree- admitting medical team. Children were excluded if they
ment. At face value, the scoring system devised by were known to have another reason for respiratory
Bierman et al. for asthma and modified by Tal et al.8 distress, for example, chronic lung disease or bronchi-
for bronchiolitis that included a 4th clinical parameter ectasis, gastroenteritis, liver function impairment, and
(cyanosis) is the most clinically appropriate and most congenital heart disease.
user-friendly. The known poor agreement of absence/
presence of wheeze (kappa 0.29),9 and other clinical
Clinical Assessment
signs on auscultation among general practitioners exam-
ining young children (kappa of 0.12–0.39),10 means Standardized data forms were used to collect demo-
that a complex system that incorporates detection of graphic, medical history and clinical information from
wheeze at various parts of the inspiration/expiratory each child. Two scoring systems were completed inde-
pendently, that is, blinded to the other assessment by a
pair of ‘‘raters’’ who were study nurses (G.M. with L.V.
ABBREVIATIONS: or G.M. with C.W.). Two nurses were experienced
aROC Area under receiver operating curve while the other was junior. Children were assessed in a
ED Emergency department calm state (i.e., no <5 minutes after a procedure or
NT Northern Territory breast feeding). Training in the use of the scoring sys-
RACS Respiratory assessment change in score tems included an education training session along with
RDAI Respiratory distress assessment instrument
RDH Royal Darwin Hospital
a written protocol.
SpO2 Oxygen saturation measured on a pulse oximeter Four specific respiratory components as described by
K Kappa Tal et al8 (RR, accessory muscle use, degree of wheez-
ing, and cyanosis) were collected. We further modified
Pediatric Pulmonology
Validated Severity Tools for Bronchiolitis 3
6
TABLE 1— Lowell et al. Score and Papers That Used This Score

Authors Components of score How validated How were scores reported?


6
Lowell et al. scores
Lowell et al.6 Composite score 0–17 Inter rater agreement Wheezing: K ¼ 0.9
Wheezing (0–8) Respiratory retractions: K ¼ 0.64
Respiratory retractions (0–9)
Schuh et al.23 Lowell et al. None Mean RDAI score
Corneli et al.24 Lowell et al. None Change in RACS
Kuyucu et al.25 Lowell et al. None Mean RDAI score
De Brasi et al. Lowell et al. None Mean RDAI score
Modified scores of Lowell et al.6 and papers that used this score
Mesquita et al.26 Lowell et al. None Mean RDAI score
Bar et al.27 Lowell et al. None Mean RDAI score
Abul-Ainine et al.28 Lowell et al. None Mean RDAI score
Klassen et al.29 Lowell et al. Inter rater agreement Overall kappa for RDAI
score 0.93 (95% CI: 0.89–0.97)
Tal et al.8 scores
Tal et al.8 Composite score (0–12) None Mean score
Wheezing (0–3)
Respiratory retractions (0–3)
Cyanosis (0–3)
Respiratory rate (0–3)
De Boeck et al.30 Tal et al. None Mean score
van Woensel et al.31 Tal et al. None Mean score
Berger et al.32 Tal et al. None Mean score
Bierman et al.18 Tal et al. None Mean score
Modified scores of Tal et al.8 and papers that used this score
Vieira et al.33 Tal et al. None Mean score
Wang et al.14 scores (bronchiolitis and pneumonia)
Wang et al.14 Composite score (0–12) Inter rater agreement Respiratory rate K ¼ 0.38,
Wheezing: K ¼ 0.31
Respiratory rate (0–3) Respiratory retractions: K ¼ 0.21
Wheeze (0–3)
Respiratory retractions (0–3)
General condition (0–3)
Postiaux et al.34 Wang et al. None Mean score
Modified scores of Wang et al.14 and papers that used this score
Beck et al.35 Wang et al. None Mean score
Other scores used
Walsh et al.20 Severity model (score not described) Inter rater agreement Wheezing: K ¼ .0.189
Respiratory retractions: K ¼ 0.304
Liu et al.4 Validated composite score (0–12) Inter rater agreement Respiratory rate: K ¼ 0.34
Age related respiratory rate (0–3) Respiratory retractions: K ¼ 0.39
Wheezing: K ¼ 0.43
Respiratory retractions (0–3) Dyspnoea: K ¼ 0.43
Wheezing (0–3)
Dyspnoea (0–3)
Kristjansson et al.15 Composite score (0–10; respiratory rate, None Mean score
respiratory retractions, cyanosis,
and wheeze general condition)

NB: Published clinical scores in the literature. Note that only scores where components were described and we could access the papers have
been included (including adaption from Gadjos paper).

this system to replace cyanosis with SpO2 (termed mod- was assessed by observing the child throughout the
ified-Tal score, Table 2). Each component scored clinical assessment. RR was counted over 60 seconds.
between 0 and 3, providing a composite score of 0–12. Accessory muscle use and SpO2 (oxygen saturation
The components used were defined to ensure standardi- measured on pulse oximetry using Philips SureSigns
zation between staff. Wheezing was defined as a high VM8) were documented after observing the child for
pitched whistling sound assessed by listening to all 60 seconds after oxygen had been turned off (if applica-
lung fields with a Littman’s II stethoscope. Cyanosis ble). Both assessors reviewed SpO2 at the same time, to
Pediatric Pulmonology
4 McCallum et al.
TABLE 2— Tal and Modified-Tal Scoring Systems

Tal scoring system

Respiratory rate
Score (breaths/min) Wheeze Cyanosis Accessory respiratory muscle utilization

0 <30 None None None (no chest in-drawing, i.e., absence of


lower part of the chest moves in or retracts
when inhalation occurs)
1 30–45 Terminal expiration only Peri-oral on crying only þ
presence of mild intercostal in-drawing (just
visible), no head bobbing or tracheal tug
2 46–60 Entire expiration and inspiration Perioral in rest þþ
with stethoscope only moderate amount of intercostal in-drawing, no
head bobbing or tracheal tug
3 >60 Entire expiration and inspiration Generalized in rest þþþ
without stethoscope only moderate or marked intercostal in-drawing
with presence of head bobbing or tracheal tug

Modified-Tal scoring system

Respiratory rate
Score (breaths/min) Wheeze SpO2 Accessory respiratory muscle utilization

0 <30 None >95 None (no chest in-drawing, i.e., absence of


lower part of the chest moves in or retracts
when inhalation occurs)
1 30–45 Terminal expiration only 94–95 þ
presence of mild intercostal in-drawing (just
visible), no head bobbing or tracheal tug
2 46–60 Entire expiration and inspiration 90–93 þþ
with stethoscope only moderate amount of intercostal in-drawing, no
head bobbing or tracheal tug
3 >60 Entire expiration and inspiration <89 þþþ
without stethoscope only moderate or marked intercostal in-drawing
with presence of head bobbing or tracheal tug

reduce the amount of time the child was off oxygen. rater agreement using weighted kappa (K), with
If the child’s SpO2 fell below the cut off of <89% descriptors described by Landis and Koch.12 Values of
SpO2, oxygen was immediately recommenced and a >0.6 was considered substantial and >0.8 almost per-
score of 3 was assigned (both remained blinded to the fect. For weighted overall kappa, the most experienced
other score). All assessments were completed within nurse’s (GM) score was used as the gold standard to
15 minutes of each other with no change in medical calculate weighted kappa using bootstrapping, and
treatment between assessments, reducing the chance of confidence intervals (95% CI). To determine whether
a clinical change in the child. the baseline score predicted the need for oxygen at 12
or 24 hr, we calculated the area under the receiver oper-
ator curve (aROC). An aROC of 0.75 was chosen to
Statistical Methods
be clinically relevant.13
Data were entered on an Access database and
analyzed using Stata version 11 (Stata Corp., College
RESULTS
Station, TX). As data were not normally distributed;
non-parametric measures were used. Participant charac- Of 138 eligible children, 23 families (17%) declined
teristics are presented as median and interquartile range participation. The median age of the 115 children en-
(IQR: 25–75% and/or range). rolled was 5.4 months (IQR: 2.9–10.4) with 75 (65%)
We examined the internal consistency of each scoring boys. More than two thirds of the study cohort 87/115
system, to establish how individual components contrib- (76%) were Indigenous and 74 (64%) lived in remote
uted to the overall score using Cronbach a coefficient. Indigenous communities. The median number of days
A score of >0.6 was regarded as good internal consis- children experienced any respiratory symptoms at time
tency. Reliability was defined in terms of good inter- of enrolment was 3 (IQR: 2–5). The median composite
Pediatric Pulmonology
Validated Severity Tools for Bronchiolitis 5
TABLE 3— Internal Consistency (Cronbach a Values) for Tal and Modified-Tal Scoring Systems and Inter-Rater
Reliability: Weighted Kappa Score Between Raters

Scoring system Weighted kappa scores (95% CI)

Variable Tal Modified-Tal Nurse 1 versus Nurse 2 Nurse 1 versus Nurse 3

Respiratory rate 0.55 0.63 0.71 (0.58, 0.84) 0.53 (0.40, 0.7)
Wheezing 0.69 0.73 0.77 (0.66, 0.88) 0.70 (0.55, 0.88)
Cyanosis 0.74 N/A 1.00a 0.91 (0.80, 1.0)
Accessory muscle use 0.62 0.68 0.78 (0.68, 0.88) 0.65 (0.51, 0.78)
SpO2 N/A 0.72 1.00a 1.00a
b b
Overall score 0.66 0.70

See Table 2 for description.


Nurse 1 and 2 (experienced nurses) and nurse 3 (junior nurse).
a
NB: where 95% CI is not described in table, perfect agreement was not analyzed.
b
N/A: Overall Kappa described in results.

score for the group was 5 (range 1–11); 27 children had however, the 95% CI were very wide and thus has
a score of 1–3, 56 scored 4–6, 29 scored 7–9, and 3 limited utility.
scored 10–11. On reviewing the various scoring systems in the
The internal consistency of the scoring systems was study of bronchiolitis (Table 1), we found a variety of
good, all components of the Modified-Tal score contrib- systems. Some utilized systems only included respirato-
uted significantly to the overall score (Table 3). Of ry distress assessment with wheezing and retractions;
the Tal score, other than RR, the other components others used modified systems that included respiratory
exceeded the cut-off of 0.6 (Table 3). rate, cyanosis, and more recently SpO2.4,6,8,14–16 The
Overall inter-rater reliability for Modified-Tal was RDAI developed by Lowell et al.6 includes only two
excellent K ¼ 0.70 (95% CI: 0.63–0.76) and also for components for assessment (wheezing and respiratory
Tal K ¼ 0.72 (95% CI: 0.63–0.83). Overall agreement retractions), whilst that developed by Wang et al.14
between raters was very good (Table 3). The lowest includes respiratory rate, wheezing, respiratory retrac-
kappa recorded was RR (K ¼ 0.53). tions, and general appearance. Both were validated only
With regard to whether the score predicted require- for inter-rater reliability and used by doctors yet in clin-
ment for supplementary oxygen at 12 and 24 hrs in the ical research, these scores (with some modification)
children (n ¼ 57) who were not on oxygen at enrol- were used by nurses and some papers provided little
ment. At 12 and 24 hrs aROCs were 0.68 (95% descriptions of training or how various raters scored.
CI: 0.13, 1.0) and 0.75 (95% CI: 0.34, 1.0), respective- Of the papers that assessed agreement of these com-
ly. Both scores had very wide confidence intervals. ponents, they varied considerably among studies. In our
From the aROC graphs, the best cut off for both time study, we found that items of individual and overall in-
points was a score of >3. For the children already on ter-rater reliability were excellent between the study
oxygen at enrolment (n ¼ 58), the Modified-Tal score nurses, often higher than other scores described. Al-
did not predict oxygen requirement at either 12 or though, the study nurses’ clinical paediatric experience
24 hrs, with an aROC of 0.60 (95% CI: 0.46, 0.75). varied considerably, the inter-rater agreement was very
good for both wheezing and respiratory retractions, K
of >0.7 and 0.65, respectively. This is unlike Wang
DISCUSSION
et al.14 and Walsh et al.’s17 findings with K values of
In 115 children with bronchiolitis, we have shown 0.189–0.31. Our high agreement score is likely related
the internal validity and reliability of both the Tal and to the training and calibration sessions in assessment of
Modified-Tal scoring systems. Both systems performed the components using a standardized protocol and edu-
well although the modified-Tal had slightly better face cation sessions (including video recordings) prior to
validity and was slightly more meaningful, with each commencement of the study. Thus, as suggested by Liu
component significantly contributing to the overall et al.4 we evaluated the Tal scoring system which was a
score. To the best of our knowledge, no other severity modified originally from Bierman and Pierson18 in our
scoring system for bronchiolitis have examined for context. We substituted SpO2 readings for cyanosis as it
internal consistency. Based on an aROC of 0.75 as a is a simple and informative part of management, and
clinically useful scoring system,13 the modified-Tal may oximeters are easily accessible. The Modified-Tal score
predict O2 requirement at 24 hrs but not at 12 hrs, was better than the Tal score. For those resource limited
Pediatric Pulmonology
6 McCallum et al.

settings where oximeters are limited, the Tal score and can be reliably used in research and clinical prac-
could feasibly be used in place of the Modified-Tal tice. However, its utility for prediction of O2 require-
score, as our results showed cyanosis had a very strong ment within 24 hrs is limited.
internal validity of 0.74 and substantial inter-rater
agreement. ACKNOWLEDGMENTS
For those children not on oxygen at enrolment, the
Modified-Tal score was predictive of oxygen require- We thank the medical and nursing staff for their on-
ment at 24 hrs with an aROC of 0.75 but not at 12 hrs going support and identifying the children for the study.
(aROC 0.68). There was however a wide confidence in- We are grateful for all the children and families who
terval thus predictability must be viewed with caution. participated in this study. Study supported by NHMRC
Our study did not aim to determine a model for predict- grant 605809 and A.C. is supported by a NHMRC prac-
ing admission as undertaken by Marlais et al.19 and titioner fellowship (grant number 545216).
Walsh et al.20 for two reasons. Firstly, our intent was to
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Pediatric Pulmonology

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