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CONCISE CLINICAL REVIEW

A Systematic Review of Tools to Measure Respiratory Rate in Order to


Identify Childhood Pneumonia
Amy Sarah Ginsburg1, Jennifer L. Lenahan1, Rasa Izadnegahdar2,3, and J. Mark Ansermino4
1
Department of Global Health, Save the Children Federation, Inc., Fairfield, Connecticut; 2Department of Pediatrics, University of
Washington, Seattle, Washington; 3Seattle Children’s Hospital, Seattle, Washington; and 4Department of Anesthesiology,
Pharmacology, and Therapeutics, The University of British Columbia, Vancouver, British Columbia, Canada

Abstract describing manual devices took place in low-resource settings,


all studies describing automated devices were conducted in
Pneumonia is the leading infectious cause of death in children well-resourced settings. Direct comparison between studies
worldwide, with most deaths occurring in developing countries. was complicated by small sample size, absence of a consistent
Measuring respiratory rate is critical to the World Health reference standard, and variations in comparison methodology.
Organization’s guidelines for diagnosing childhood pneumonia in There is an urgent need for affordable and appropriate innovations
low-resource settings, yet it is difficult to accurately measure. We that can reliably measure a child’s respiratory rate in low-resource
conducted a systematic review to landscape existing respiratory settings. Accelerating development or scale-up of these technologies
rate measurement technologies. We searched PubMed, Embase, could have the potential to advance childhood pneumonia diagnosis
and Compendex for studies published through September 2017 worldwide.
assessing the accuracy of respiratory rate measurement technologies
in children. We identified 16 studies: 2 describing manual devices Keywords: respiratory rate; childhood pneumonia; automated;
and 14 describing automated devices. Although both studies technology; low-resource settings

Pneumonia remains the leading infectious of the Integrated Management of breathing rapidly. Inaccurate or imprecise
cause of death among children younger Childhood Illness and iCCM criteria is the measurements can stem from factors including
than 5 years of age. In 2015, pneumonia accurate classification of fast breathing, poor visibility of the start or end of a breath,
accounted for 16% of child deaths globally defined as 60 or more breaths per minute in an irritable or moving child, or difficulty
(1). Although childhood pneumonia deaths infants younger than 2 months, 50 or more counting or remembering the count (7).
can be prevented with simple interventions breaths per minute in infants aged 2 to 11 Accurate assessment of RR is critical in
and appropriate treatment, pneumonia months, and 40 or more breaths per minute low-resource settings where other diagnostic
often goes undiagnosed and untreated in in children aged 12 to 59 months (4). tools, such as pulse oximetry or chest
the community until the child is severely In low-resource settings, counting the radiography, are typically not available and
ill (2, 3). In low-resource settings, number of breaths typically is performed pneumonia is diagnosed based on the child’s
pneumonia is diagnosed using the manually with the aid of watches, timers, clinical signs alone. Given the high burden
World Health Organization Integrated and counting beads (5, 6). However, even and mortality of childhood pneumonia,
Management of Childhood Illness and with these counting aids, measuring a there is growing demand for better ways
Integrated Community Case Management child’s respiratory rate (RR) through to measure RR accurately and reliably.
(iCCM) guidelines, which rely on the visual observation requires focused Although there are numerous existing and
appreciation of subjective clinical signs concentration and can be challenging in potential approaches for measuring RR
and symptoms. An important component a child who may be moving, crying, or (Table 1), it is important to assess whether

( Received in original form November 12, 2017; accepted in final form February 23, 2018 )
Author Contributions: A.S.G.: study design, search term development, device category development, literature search, article review and analysis, table and
figure design, and manuscript writing and editing; J.L.L.: literature search, article review and analysis, table and figure design, and manuscript writing and
editing; R.I.: manuscript review and editing; and J.M.A.: manuscript writing, review, and editing.
Correspondence and requests for reprints should be addressed to Jennifer L. Lenahan, M.P.H., 501 Kings Highway East, Suite 400, Fairfield, CT 06825. E-mail:
jlenahan@savechildren.org.
CME will be available for this article at www.atsjournals.org.
Am J Respir Crit Care Med Vol 197, Iss 9, pp 1116–1127, May 1, 2018
Copyright © 2018 by the American Thoracic Society
Originally Published in Press as DOI: 10.1164/rccm.201711-2233CI on February 23, 2018
Internet address: www.atsjournals.org

1116 American Journal of Respiratory and Critical Care Medicine Volume 197 Number 9 | May 1 2018
CONCISE CLINICAL REVIEW

Table 1. Respiratory Rate Method Categories

Manual Methods Description Examples*

Manual count
Timers only Analog devices used to inform the observer when to ARI timer, wristwatch
start and stop counting breaths.
Assisted count
Counters only Color-coded string of beads used in combination with Breath Abacus, International Rescue Committee
a timer to eliminate the need for an observer to counting beads
remember breath count and age-designated cutoff
rates.
Combined timer and Stand-alone digital devices or software-based mobile Mobile software applications
counter applications with a built-in 1-min timer to eliminate
the need for an observer to remember breath count
by having the user press a button or tap the screen
to register each breath.

Automatic Methods Description Examples*

Exhaled breath
Humidity RR derived from oronasal moisture sensors measuring Interferometry sensors, relative humidity sensors,
fluctuations in humidity with respiration. absolute humidity (moisture) sensors,
hygrometers
Temperature RR derived from oronasal temperature sensors Thermistors, infrared thermography, thermocouple
measuring fluctuations in temperature with sensors, nasal prongs, face masks
respiration.
Air pressure RR derived from oronasal sensors measuring Barometric pressure sensors, pressure transducers,
fluctuations in air pressure with respiration. airflow velocity sensors, spirometers,
pneumotachometers
ETCO2 RR derived from oronasal capnography sensors Capnometers, mid-infrared LED detectors
measuring fluctuations in carbon dioxide
concentrations with respiration.
ETO2 RR derived from oronasal oxygen sensors measuring Differential paramagnetic sensors, fiber optic
fluctuations in oxygen concentrations with respiration. fluorescence-based oxygen sensors, gas analysis
systems
Thoracic effort
Thoracic RR derived from sensors measuring fluctuations in Inductance plethysmography sensors, piezoelectric
circumference thoracic circumference with respiration. sensors, rubber dilation sensors, stretch sensors,
chest straps, or belts
Thoracic motion RR derived from sensors measuring fluctuations in Accelerometers, gyroscopes, ballistocardiography
thoracic motion with respiration. sensors, bioradiolocation sensors, noncontact
microwave and wireless networks, ferroelectric
sensors, mattress sensors, electromagnetic
generator, small movement motion amplification
programs
VT RR derived from electrodes measuring fluctuations in Bioimpedance electrode sensors varying in
lung volume with respiration. presentation (disposable skin adhesive, portable
body-worn devices, wearable garments)
Respiratory sounds
Oronasal RR derived from acoustic respiratory signals Noncontact microphones or wearable headsets
measured near the oronasal area.
Thoracic RR derived from acoustic respiratory signals Electronic auscultation of signals collected from
measured near the chest, back, or armpit. modified digital stethoscopes
Tracheal RR derived from acoustic respiratory signals Sensor adhesives placed near the throat or neck
measured near the throat or neck.
(Continued )

Concise Clinical Review 1117


CONCISE CLINICAL REVIEW

Table 1. (Continued )

Automatic Methods Description Examples*

Indirect effects on
cardiovascular
physiology/blood
flow
ECG RR derived indirectly from the ECG measured by a Numerous portable ECG electrode systems
configuration of electrodes. integrating patented signal extraction techniques
PPG RR derived indirectly from the PPG measured by a pulse Numerous portable pulse oximetry systems
oximeter. integrating patented signal extraction techniques,
including finger clip sensors and wrist-worn
monitors, among others
PtcCO2 RR derived indirectly from the PtcCO2 measured by a wet CO2 measured potentiometrically by determining
Ag/AgCl electrode heated above fevered the pH of an electrolyte layer and used to
temperatures. calculate RR
PAT RR derived indirectly from the PAT waveform measured Fusion algorithms process PAT waveforms to
by an apparatus capable of sensing finger pulsatile identify respiratory events used to calculate RR
arterial volume changes.
ABP RR derived indirectly from the ABP measured by a Complete health monitoring systems displaying vital
sphygmomanometer. signs (e.g., ABP, pulse, and temperature) in
addition to RR

Definition of abbreviations: ABP = arterial blood pressure; ARI = acute respiratory infection; ETCO2 = end-tidal carbon dioxide concentration; ETO2 = end-
tidal oxygen concentration; LED = light-emitting diode; PAT = peripheral arterial tonometry; PPG = photoplethysmogram; RR = respriatory rate.
*Examples provided are for illustrative purposes and are not claimed to be complete.

these have been rigorously evaluated in describing accuracy of assessment of breath were extracted into a database with
a way that facilitates comparisons of count or RR in spontaneously breathing designated fields: author, title, publication
accuracy and performance. This systematic human infants and/or children younger date, journal, country/countries of study,
review provides an overview of the RR than 5 years of age compared with a population(s) studied, study setting (e.g.,
measurement tools that have undergone a reference standard. The exclusion criteria laboratory, hospital, field), sample size, time
clinical evaluation of accuracy against a included mechanically ventilated subjects, period, study type, primary objective,
reference standard among spontaneously nonhuman animal subjects, failure to categorization of device as manual
breathing children younger than 5 years of report RR values, lack of a reference or automated, reference standard,
age. Some of the results of these studies standard, no assessment of accuracy, non- measurement interval, who took the
have been previously reported in the form English publication, subjects older than 5 measurement (e.g., research team, nurse),
of an abstract (8). years of age, inability to disaggregate data outcome measure, and statistical method of
on children younger than 5 years from data comparison. Included studies were divided
on older children and/or adults, inability into two groups on the basis of how the
Methods to disaggregate data on mechanically devices measured RR: manually by an
ventilated children from data on non– observer or automatically recording from a
Search Strategy and Selection mechanically ventilated children, review physical measurement. Manual methods
Criteria article reporting secondary data, and were further categorized as manual count
PubMed, Embase, and Compendex/ insufficiently detailed description of (timers only) or assisted count (combined
Engineering Village were searched through methods. If not explicitly stated, study timer and counter) (Table 1). Automated
September 2017 for English-language authors were contacted for confirmation technologies were categorized based on
publications reporting on measuring or that subjects were spontaneously breathing the physiological parameter from which
monitoring RR in infants and children and not mechanically ventilated. For this the measurement was obtained: exhaled
younger than 5 years of age. The search review, accuracy is defined as the difference breath (humidity, temperature, air pressure,
strategy used preferred indexing terms between the values measured by the carbon dioxide, oxygen), thoracic effort
from each database and was built around a experimental device and the “true value” as (circumference, motion, volume), respiratory
set of controlled vocabulary terms and quantified by the reference standard. sounds (oronasal, thoracic, tracheal), and
relevant text words in the title, abstract, or indirect effects on cardiovascular physiology
subject fields (or a combination of those fields). Data Extraction and Analysis (electrocardiogram, photoplethysmogram
Articles were screened by two team Included articles were critically appraised [PPG], transcutaneous partial pressure of
members for relevance to the analysis on the for eligibility criteria and clearly described carbon dioxide, peripheral arterial
basis of sequential review of study titles, methods following Preferred Reporting tonometry, arterial blood pressure).
abstracts, and full text. The inclusion criteria Items for Systematic Reviews and Meta- All data were analyzed qualitatively by
were specified as English publications Analyses guidelines (9). The following data assessing the device category, method of

1118 American Journal of Respiratory and Critical Care Medicine Volume 197 Number 9 | May 1 2018
CONCISE CLINICAL REVIEW

evaluation, and accuracy in comparison to a (10–23). Both papers on manual devices (6). Formative research in Ghana suggested
reference standard. An objective of this reported data from low-resource settings, that color-coded beads could facilitate
review was to pool outcome measures across with one conducted in India and the classification accuracy by assisting
studies through meta-analytic methods. other consolidating evidence from studies community health workers (CHWs) in
However, the dearth of studies reporting like in Ghana, South Sudan, and Uganda identifying fast breathing by age without
outcomes precluded this type of quantitative (Table 2) (6, 24). the need to remember age-specific cutoff
analysis. rates. Pooled data from studies among
primarily illiterate CHWs in South Sudan
Manual Devices and Uganda indicate a 41% absolute
Results The two publications describing the increase in the accuracy of fast breathing
accuracy of fast breathing assessment using classification when assisted by counting
Studies Included through Systematic manual devices included primarily low beads in conjunction with a timer
Review literacy, community-based, frontline compared with an acute respiratory
From a total of 7,669 unique citations, providers in low-resource settings and used infection timer alone (odds ratio [OR],
89 publications were identified as a reference standard of clinician count over 5.7; P , 0.005) (Table 2). In South Sudan,
sufficiently relevant for full text review, 1 minute (Table 2). In a study conducted in the use of counting beads enabled 60% of
and 16 were ultimately included India in the early 1990s, the accuracy of fast illiterate CHWs to accurately classify fast
(Figure 1). Fourteen of those papers breathing assessment by 10 traditional birth breathing. In Uganda, findings differed
reported on automated devices, and two attendants was higher when assisted by age- based on the literacy level of the CHWs.
reported on manual devices (Table 2). All specific color-coded counting beads in Among illiterate CHWs, the ability to
included studies on automated devices comparison to no device (82 vs. 60%) (24). classify fast breathing increased from 37%
reported data from well-resourced settings, In more recent years, studies assessing the using the timer alone to 73% using the
including the United Kingdom (n = 4), relative benefit of counting beads in timer and counting beads combined (OR,
Sweden (n = 3), the Netherlands (n = 3), the conjunction with an acute respiratory 4.4; P , 0.005). However, literate CHWs
United States (n = 1), Israel (n = 1), infection timer have been conducted to were 5.6 times as likely to report a breath
Switzerland (n = 1), and Australia (n = 1) inform iCCM guidelines on pneumonia count within plus or minus two breaths of
the reference standard when assisted with
a timer alone compared with a timer in
conjunction with counting beads (OR, 5.6;
Records identified through database
searches P , 0.001). A mobile phone application
(n = 9,367) was also assessed in this study, and no
significant difference in accuracy was
noted between the timer and the mobile
phone application (OR, 1.1; P = 0.08) (6).
Records after duplicates removed
Among literate CHWs using any method,
(n = 7,669) breath count was typically more accurate
at slower breathing rates rather than faster
rates, and CHWs tended to overestimate
RR in the slow-rate scenario and
underestimate RR in the fast-rate scenario.
Records after abstracts screened
(n = 89) Automated Devices
We identified 14 studies assessing the
accuracy of automated breath counters
(Table 2). One study assessed multiple
Full-text articles excluded (n = 75)
devices, for a total of 15 technologies
-No measure of RR accuracy reported (n = 36)
-Subjects 5 years of age (n = 16)
assessed. Automated breath counters
-Unable to disaggregate data on children <5 fell into four categories: indirect effects
from older age groups (n = 9) on cardiovascular physiology/blood flow
-Subjects mechanically ventilated (n = 6)
-Insufficiently described methods (n = 5)
(n = 8); thoracic effort, VT (n = 3); thoracic
-Review article (n = 2) effort, thoracic motion (n = 3); and
-Not published in English (n = 1) exhaled breath humidity (n = 1) (Table 2).
Indirect effects on cardiovascular
physiology/blood flow. Two studies describing
PPG took place in a neonatal ICU (NICU)
Studies included in review in Sweden, using transthoracic impedance
(n = 16)
(TTI) plethysmography as the reference
standard (10, 11). In one study, a
Figure 1. Systematic review flow diagram. RR = respiratory rate. PPG probe, designed to cover a small skin

Concise Clinical Review 1119


Table 2. Respiratory Rate Measuring Methods Evaluated for Accuracy in Children Younger Than 5 Years of Age

1120
Location, Users, Reference
Author, Year Device Category Setting Subjects Standard Results

Manual
Bang and Bang, Breath Counter Assisted count, India, household Users: TBAs (n = 10); Physician count, 82% TBAs accurately
1992 (24) counting beads counter only subjects: children 1 min identified fast breathing
,5 yr (n = 5) using Breath Counter,
compared with 60%
accuracy without using
Breath Counter (P , 0.05).

Noordam et al., Study 1: ARI timer vs. Assisted count, Study 1: South Study 1: Users: CHWs Physician count, Study 1: Illiterate CHWs 5.7
2015 (6) ARI timer and combined timer and Sudan and (n = 65); subjects: 1 min (accuracy times as likely to accurately
counting beads counter Uganda, children 2–59 mo window 63 breaths classify fast breathing when
household (n = 65) for Study 1 and using ARI timer and
Study 2, 62 breaths counting beads together
for Study 3) compared with using ARI
timer alone (OR, 5.7;
P , 0.005).
Study 2: Counting Study 2: South Study 2: Users: CHWs Study 2: Among illiterate
beads Sudan, hospital (n = 27); subjects: CHWs, 60% accurately
children 2–59 mo classified fast breathing
(n = 69) using counting beads.
Study 3: ARI timer vs. Study 3: Uganda, Study 3: Users: CHWs Study 3: Literate CHWs 5.6
ARI timer and virtual (video) (n = 94); subjects: times as likely to accurately
counting beads; ARI video case series classify fast breathing when
timer vs. mobile (each CHW shown using ARI timer alone,
phone application in two children with compared with using ARI
which button fast breathing and timer and counting beads
pressed for every one without) together (OR, 5.6; P ,
breath observed, 0.001). No significant
and which beeped difference in accuracy
after 1 min between ARI timer and
mobile phone application
(OR, 1.1; P = 0.08).

Automatic
Johansson et al., PPG Indirect effects on Sweden, NICU Users: research team; TTI, 30 s PPG signal 2.7% (SD, 61.1%)
1999 (10) cardiovascular subjects: neonates false-negative breaths and
physiology/blood (n = 6) 1.5% (SD, 60.4%)
flow false-positive breaths
(Continued )
CONCISE CLINICAL REVIEW

American Journal of Respiratory and Critical Care Medicine Volume 197 Number 9 | May 1 2018
Table 2. (Continued )

Location, Users, Reference


Author, Year Device Category Setting Subjects Standard Results

Olsson et al., PPG at three Indirect effects on Sweden, NICU and Users: research team; TTI, 30 s Strong association between
2000 (11) monitoring sites cardiovascular neonatal subjects: infants RR recorded by PPG and
(leg, buttock, and physiology/blood intermediate (n = 10) RR recorded by TTI at all
IR) flow care unit three sites, with correlation
coefficients as follows:

Concise Clinical Review


Leg: 0.995 (95% CI,
0.980–0.999)
IR: 0.997 (95% CI,
0.988–0.999)
Buttock: 0.995 (95% CI,
0.980–0.999)

Neuman et al., CHIME device, Indirect effects on United States, Users: research team; Human observer Sensitivity: 96%
CONCISE CLINICAL REVIEW

2001 (12) which measures cardiovascular home (data subjects: infants using Specificity: 65%
RR using physiology/blood collection) and (n = 20) simultaneously
Respitrace Plus flow CHIME base recorded CO2 and
RIP station oronasal air
(interpretation) temperature
(thermistor probe)
to identify breaths,
5 min

Roback et al., FORE FORE: exhaled Sweden, NICU Users: research team; Manual count (1 min, FORE: Mean bias, 23.4%;
2005 (13) breath, humidity subjects: neonates repeated every 6 deviation from reference of
(n = 17) min until at least more than 20% in 22.7%
8 recordings were observations
obtained)
TTI TTI: thoracic effort, VT TTI: Mean bias, 21.6%;
deviation from reference of
more than 20% in 23.8%
observations

Wertheim et al., Pleth trace Indirect effects on United Kingdom, Users: research team; Respiratory airflow Median difference (pleth
2009 (14) cardiovascular postnatal subjects: infants measured using 2 flow), 20.01 breaths/min
physiology/blood hospital ward (n = 14) low–dead space (range, 25.84 to 0.76;
flow ultrasonic flowmeter P = 0.802). Mean difference
connected to face (pleth 2 flow) using Bland-
mask, 2 min Altman analysis, 20.82
breaths/min. Using 1 Hz
LPF to generate a
respiratory-like trace,
median difference, 20.89
breaths/min (range, 28.41
to 0.38; P = 0.038).
(Continued )

1121
Table 2. (Continued )

1122
Location, Users, Reference
Author, Year Device Category Setting Subjects Standard Results

Wertheim et al., Pleth recordings Indirect effects on United Kingdom, Users: research team; Manual count by Analysis of pleth within 10
2013 (15) cardiovascular inpatient subjects: acutely direct observation breaths/min of manual
physiology/blood hospital unit wheezy children of chest wall count in 15 of 18 children
flow aged 1–4 yr (n = 18) movement, 30 s during acute wheezing
and 15 of 16 children at
follow-up. Using paired t
test, no significant
difference between pleth
and manual count during
acute wheezing or
follow-up.

Petrus et al., Tidal breathing Thoracic effort, VT Switzerland, Users: research team; Ultrasonic flowmeter Mean difference (vest 2 mask),
2015 (16) flow–volume loop hospital subjects: healthy with face mask 0.71 breaths/min (95% CI,
measurements infants (n = 19); (Spiroson) 0.24–1.17; P = 0.031).
using vest-based infants with lung
inductive disease (n = 18)
plethysmograph
system (FloRight)

Kohn et al., 1. Transthoracic Thoracic effort, VT Israel, NICU Users: research team; Manual count using Tight correlation between
2016 (17) impedance subjects: premature video recording of motion sensor modality and
continuously infants (n = 9; 11 chest and abdomen visual count (r2 = 0.83), with
monitored via sessions) (1-min span slope of 0.96, very close to
standard pediatric counted every 5 min) line of equality.
chest electrodes Impedance-based RR
determinations had lower
2. Continuous correlation with manual count
monitoring of (r2 = 0.65) and larger deviation
respiratory from expected line of equality.
dynamics and
measurement
of local tidal
displacement using
three motion
sensors attached
to both sides of
chest wall and
upper abdomen

Shah et al., PPG using modified Indirect effects on United Kingdom, Users: research team; Manual count by Mean absolute error
2015 (18) autoregressive cardiovascular hospital subjects: children nurse (15 or 30 s) in breaths per minute
modeling; RR physiology/blood emergency aged 0–5 yr (n = between intervention and
measured over 60-s flow department 126) reference, 7.6.
sliding window with Median absolute error, 6.0.
50-s overlap
(Continued )
CONCISE CLINICAL REVIEW

American Journal of Respiratory and Critical Care Medicine Volume 197 Number 9 | May 1 2018
Table 2. (Continued )

Location, Users, Reference


Author, Year Device Category Setting Subjects Standard Results

Kraaijenga et al., dEMG; 1-h recording Thoracic effort, Netherlands, NICU Users: research team; Chest impedance, RR measured by dEMG
2015 (19) taken on Days 1, 3, thoracic motion subjects: preterm measured at same significantly correlated to
and 7; calculated infants (n = 31) time points as chest impedance (r = 0.85;
mean RR from dEMG P , 0.001). Bland-Altman
1-min time intervals plot between techniques

Concise Clinical Review


at six fixed time with mean difference of
points (5, 15, 25, 35, 22.3 breaths/min.
45, and 55 min)
van Gastel et al., Noncontact camera Indirect effects on Netherlands, NICU Users: research team; Overall performance CHROM strongest performer
2016 (20) detecting cardiovascular subjects: neonates compared with of four algorithms, with
respiratory-induced physiology/blood (n = 2; 20 videos ECG-derived correlation coefficient (r) of
color differences of flow analyzed) respiratory signal. 0.87 and mean absolute
CONCISE CLINICAL REVIEW

the skin; two remote CHROM and error of 4.67 breaths,


PPG algorithms PBV algorithms compared with
used: CHROM and compared with ECG-derived respiratory
PBV two benchmark signal.
PPG-based
algorithms

Seddon et al., Pleth trace Indirect effects on United Kingdom, Users: parents; RIP bands Median difference (RIP 2 pleth),
2016 (21) cardiovascular home subjects: healthy 0 (range, 21.75 to 6.5
physiology/blood preterm infants with breaths/min). Bland-Altman
flow no respiratory plot indicated no difference
disease (n = 12); in accuracy at higher rates.
preterm infants who
subsequently
developed chronic
lung disease of
prematurity (n = 9)

Janssen et al., VRM system Thoracic effort, Netherlands, NICU Users: research team; Contact-based Average accuracy of VRM in
2016 (22) thoracic motion subjects: neonates thoracic impedance close-view and wide-view
(n = 2; 20 videos) plethysmography videos among neonates,
(ECG) 88.7 and 92.6%,
respectively.

Al-Naji and Thermal camera Thoracic effort, Australia, setting Users: research team; Visual count using Correlation analysis between
Chahl, 2016 using a motion thoracic motion not stated subject: 8-mo-old input video experimental device and
(23) magnification infant (n = 1) reference carried out using
technique to PCC and SRC (PCC, 0.966;
magnify breathing SRC, 0.9566).
movement (15-s Reproducibility coefficient,
video clips) 0.67 breaths/min (2.8%) and
mean difference (bias) 0.21,
with limits of agreement
10.88 and 20.46.

Definition of abbreviations: ARI = acute respiratory infection; CI = confidence interval; CHIME = Collaborative Home Infant Monitor Evaluation; CHROM = chrominance-based; CHW =
community health worker; dEMG = transcutaneous electromyography; FORE = fiberoptic respirometry; IR = interscapular region; LPF = low-pass filtering; NICU = neonatal ICU; OR = odds
ratio; PBV = pulse blood volume; PCC = Pearson correlation coefficient; pleth = pulse oximeter plethysmogram; PPG = photoplethysmogram; RIP = respiratory inductance plethysmograph;
RR = respiratory rate; SRC = Spearman Rho coefficient; TBA = traditional birth attendant; TTI = transthoracic impedance; VRM = video respiration monitoring.

1123
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surface area while still having a sufficiently bands as the reference standard, the Bland- was 0.71 breaths/min (95% confidence
large detector area, was attached to Altman plot indicated no difference in interval, 0.24–1.17; P = 0.031) (16).
neonates’ skin on the lateral left thigh, and accuracy at higher rates, and the median Thoracic effort, thoracic motion.
RR was extracted using a band-pass filter. difference was 0 (21). Thoracic motion was captured using
When compared with the reference, the In a study evaluating PPG recordings transcutaneous electromyography to
PPG signal included 2.7% (61.1%) false- using modified autoregressive modeling calculate RR among preterm infants in a
negative breaths and 1.5% (60.4%) false- among children aged 0 to 5 years of age NICU in the Netherlands. Using chest
positive breaths (mean 6 SD) (10). In presenting at a hospital emergency impedance as the reference standard,
another study, PPG was used to assess RR department in the United Kingdom, and RR measured by transcutaneous
at three monitoring sites (i.e., leg, buttock, using manual count as the reference electromyography was significantly
and interscapular region). A strong standard, the mean absolute error was 7.6 correlated to chest impedance (r = 0.85; P ,
association between RR recorded by PPG breaths/min and the median absolute error 0.001). The Bland-Altman plot between
and RR recorded by TTI was noted at all was 6.0 breaths/min (18). Finally, a study techniques showed a mean difference of
three sites, with the highest correlation in using a noncontact camera to detect 22.3 breaths/min (19). In another NICU-
the interscapular region (correlation respiratory-induced color differences of the based study in the Netherlands, a video
coefficient, 0.997; 95% confidence interval, skin among a sample of neonates in a respiration monitoring system was used to
0.988–0.999) (11). NICU in the Netherlands, and using an assess RR among neonates. With contact-
A device developed for the ECG-derived respiratory signal as the based thoracic impedance plethysmography
Collaborative Home Infant Monitor reference standard, the camera method as a reference, the average accuracy of the
Evaluation (CHIME) project in the United demonstrated a mean absolute error of 4.67 video system in close-view and wide-view
States involving multiple components breaths/min and a correlation coefficient of among neonates was, respectively, 88.7 and
including a pulse oximeter, a thoracic 0.87 (20). 92.6% (22). In a study from Australia,
impedance monitor, and a Respitrace Plus Thoracic effort, VT. To measure VT to a thermal camera using a motion
respiratory inductance plethysmography (RIP) assess RR, TTI was used among a sample of magnification technique was used to
device collected data from infants at their neonates hospitalized in a NICU in Sweden, identify respirations in 15-second video
homes, and data was analyzed at the CHIME using manual count as the reference clips taken from a single 8-month-old
base station. Compared with a human standard. TTI demonstrated a mean bias of infant. Using visual count from the same
observer using simultaneously recorded CO2 21.6%, and a deviation from the reference input video as the reference standard,
and oronasal air temperature to identify of more than 20% was found in 23.8% of correlation analysis between the
breaths, the CHIME monitor was found to observations. The accuracy of TTI was experimental device and the reference was
have 96% sensitivity and 65% specificity (12). subject dependent, with decreased accuracy performed using Pearson correlation
Three additional studies assessed the during body movement, and TTI tended to coefficient and Spearman Rho coefficient
accuracy of RR detection using a pulse overestimate because of motion artifacts (Pearson correlation coefficient, 0.966;
oximeter plethysmographic (pleth) trace (13). In another study among a sample of Spearman Rho coefficient, 0.9566). The
(14, 15, 21). In a study analyzing pleth premature infants in a NICU in Israel, two reproducibility coefficient was 0.67
traces among infants in a postnatal hospital methods to assess RR were used 1) TTI breaths/min (2.8%) and the mean
ward in the United Kingdom and continuously monitored via standard difference was 0.21 (23).
comparing to the reference standard of pediatric chest electrodes, and 2) Exhaled breath, humidity. To assess the
respiratory airflow measured using an continuous monitoring of respiratory humidity of exhaled breath to measure RR
ultrasonic flowmeter connected to a face dynamics and measurement of local tidal among neonates in a NICU in Sweden and
mask, the median difference was 20.01 displacement using motion sensors using manual count as the reference, fiber
breaths/min and the mean difference (using attached to the chest wall and upper optic respirometry found a mean bias of
Bland-Altman analysis) was 20.82 abdomen. Using manual count via video 23.4% and a deviation from the reference of
breaths/min (14). In a study analyzing pleth recording as the reference standard, a tight more than 20% in 22.7% of observations.
traces among acutely wheezy children in an correlation was obtained between the The accuracy of fiber optic respirometry
inpatient hospital unit in the United motion sensor modality and the visual was found to be subject dependent, with
Kingdom, analysis of pleth was within 10 count (r2 = 0.83), with a slope of 0.96. The decreased accuracy during body movement,
breaths/min of the manual count by direct impedance-based measurements had a and tended to underestimate RR because of
observation reference standard in 15 of 18 lower correlation with the manual count probe displacement (13).
children during acute wheezing and in 15 of (r2 = 0.65) and a larger deviation from the
16 children at follow-up. Using a paired t expected line of equality (17). In a study
test, there was no significant difference among both healthy infants and infants Discussion
between pleth and manual count during with lung disease in a hospital setting in
acute wheezing or follow-up (15). In Switzerland, a FloRight vest–based Given the immense burden of childhood
another study from the United Kingdom inductive plethysmograph system was used pneumonia and the fact that RR is the
assessing the accuracy of pleth traces using to collect tidal breathing flow–volume loop primary method for diagnosing pneumonia
home recordings of both healthy preterm measurements to assess RR. Using an in low-resource settings, it is critical
infants and preterm infants with chronic ultrasonic flowmeter with a face mask as to understand the landscape of RR
lung disease of prematurity and using RIP the reference standard, the mean difference measurement technologies. This systematic

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review identified 3 manual and 15 to manual count include distraction, an of less than 2.5 breaths/min at 20
automated RR counting devices evaluated agitated or crying child, and mistaking breaths/min appears technically achievable,
for accuracy among spontaneously nonrespiratory movements and sounds as the current cutoff of 62 breaths/min may
breathing children younger than 5 years of breaths (13, 18, 25). Furthermore, if the be too strict, given the aforementioned
age. Although automated technologies were premise of evaluating RR measurement challenges in starting and stopping
divided a priori into 4 categories and 16 technologies is to develop a device that times (30).
subcategories (Table 1), only 4 of the improves on the accuracy of manual count, In well-resourced settings, measuring
subcategories were identified in this review: one would need a reference standard RR and other vital signs can be achieved
PPG (n = 8), VT (n = 3), thoracic motion accepted as more accurate than manual in multiple ways, sometimes involving
(n = 3), and exhaled breath humidity (n = 1) count. In the absence of a gold standard for sophisticated and expensive sensors and
(Table 2). Although devices in other RR measurement, we would recommend signal processing. However, the greatest
categories may be in the development or that future RR accuracy assessments need for accurate RR technologies is in low-
evaluation stage, these four categories include a clear indication of the start of the resource settings, where such high-cost
represent devices whose accuracy has been breath count and that the repeatability of technologies may not be appropriate or
assessed against a reference standard. No the reference standard, whether it be feasible. Although all of the manual devices
devices in the respiratory sounds category manual count, auscultation, video assessed were evaluated in low-resource
were identified in this review. Acoustically recordings, and/or capnography, be settings, all of the automated devices were
derived respiratory devices may be subject evaluated with simultaneous observations tested in well-resourced settings, often in
to signal artifact, leading to difficulties in and methods. This methodology will allow tightly controlled environments. In the
obtaining an accurate count. On the basis for the estimation of the measurement error absence of validation in low-resource
of the devices identified in this review, relative to the device accuracy. settings, it is difficult to assess the strengths
promising RR technologies include The appropriate methods and the and weaknesses of the devices included in
noncontact devices, those that can detect challenges involved in measuring this review. However, low-cost devices with
changes in motion or color among children agreement between a clinical standard and multiple uses (including the CHIME
of a range of ages and skin tones, and those a new device have previously been monitor and those that assess RR using a
that may be integrated into an existing described in detail (26, 27). With regard to pulse oximeter) may have an advantage
device like a pulse oximeter or a multiuse statistical methods, we would suggest that over single-purpose devices, because they
device such as a tablet or smart phone. the accuracy of RR measurement be would allow providers to assess multiple
A rigorous evaluation of accuracy reported as the root-mean-square vital signs with a single device, potentially
is necessary to validate any technology deviation between measured values and reducing the complexity and training
before widespread use as a diagnostic tool. reference values over a range of RRs (as is involved in incorporating a new technology
Although all studies in this review included done with devices such as pulse into clinical care.
an assessment of accuracy, there was wide oximeters). It should be clearly stated It is critical that RR devices are
variation in reference standard selection and whether observations were independent developed with the needs of low-resource
statistical methods of comparison. This (more than one observation per subject). settings in mind and should be validated in
variation precluded the ability to compare Although there is no currently accepted the settings where they will ultimately be
devices head-to-head and complicated reference standard for RR, an indication of used. In-country stakeholders and CHWs
attempts to develop standard criteria or a test–retest reliability of the standard (the should be consulted during the planning
cutoff for determining accuracy. Among the variation in measurements taken by a and development phases, as they may
studies evaluating automated technologies, single person or instrument on the same provide different perspectives (31).
reference standards included manual count subject) would give an indication of Characteristics of an RR counter most
(n = 5), TTI (n = 2), ECG (n = 2), ultrasonic precision. promising for advancement include
flowmeter connected to face mask (n = 2), Another factor to consider is the portability, durability, and low cost
RIP bands (n = 1), chest impedance (n = 1), definition of an accurate RR count. The (Table 3). The RR device should be simple
and human observer using simultaneously current UNICEF target product profile for to use and should provide the result in a
recorded CO2 and oronasal air temperature acute respiratory infection diagnostic aids way that a CHW or the child’s caregiver
to identify breaths (n = 1). This variation in requires that the “accuracy of obtained RR can understand (31, 32).
reference standards made interpreting the should be at least 62 breaths per minute The manual count assessments
accuracy of the experimental devices when compared with the number of identified in this review targeted lower-level
challenging, because the accuracy of the respiratory cycles measured over a period providers like CHWs and traditional birth
reference standards themselves was not of 60 seconds” (28). If a child is breathing at attendants as the users of the device. In
clear. Consensus regarding an appropriate 20 breaths/min, a single missed breath at contrast, in all but one of the automated
reference standard would improve the the start or end of counting (due to the device evaluations, research team members
generalizability of future RR device variation in the count’s start/end time) would were the users; the exception was a study
evaluations. account for this 2% error. This was confirmed of pulse oximeter pleth trace, in which
Although manual breath count was the in a study that measured RR twice over a parents were the users. As RR technologies
most common reference standard in this 10-minute period with the same observer and move further along in development and
review, it is known to have issues with found a mean difference of 1.8 breaths/min validation, it will be important to determine
accuracy and reliability (13, 18). Challenges (29). Although a root-mean-square deviation the level of training required for accurate use

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Table 3. Performance Needs for Respiratory Rate Counter Technologies literature, and we were not able to verify
whether the RR counters highlighted
here have moved beyond the concept or
Reliability Automatically and accurately measures respiratory rate development phase. Although some of the
Noninvasiveness Easily placed on and tolerated by an infant or child for the included RR counters did list costs, cost
shortest time possible
estimates were not always available and were
Affordability Low cost excluded from this analysis. Because this
Simplicity Simple and intuitive to use review focuses on accuracy, it does not
Cultural appropriateness Result can be understood by caregiver address reliability, feasibility, usability, and
Portability Compact, lightweight, and portable acceptability. However, these factors are
Durability Robust, dust- and water-resistant important to evaluate and consider when
Sustainability Independent and long-lasting power source introducing a new technology.
Customization Credible and culturally acceptable Finally, although this systematic review
Minimalism Least essential hardware and appropriate for low-skilled was not prospectively registered, several
community health workers steps were taken to minimize selection bias.
Validation Prototype refined and demonstrates significant progress The inclusion and exclusion criteria were
throughout product development cycle developed a priori, and an effort was
Integration Leverages a multipurpose-built platform to provide an integrated made to minimize ambiguity within these
diagnostic toolkit criteria. Two individuals screened the
citations for inclusion in this review to
Based on information in Reference 32.
reduce the risk of biased study decisions.
All decisions regarding inclusion or
exclusion of each citation were thoroughly
as well as the appropriate amount of distress the child, which could impact the documented (36).
information to present. Whether the RR child’s breathing pattern (13, 22, 34).
device should present only the breath count Movement-based RR counter technologies
or whether it should identify tachypnea can be vulnerable to motion artifacts. Conclusions
depends on the training of the end user and The challenge is to separate respiratory Assessment of RR is integral to the
the needs of the setting. If the device does from nonrespiratory signals, including pneumonia diagnostic pathway in low-
identify tachypnea, the device should be agile discriminating a moving child from a resource settings. Accelerating the
enough to have settings that may be adapted breath movement or a cry from a breath development of innovations and spurring
if guidelines change globally or regionally. sound (13, 19, 20). Technologies that the adaptation of current devices could
In performing a landscape analysis calculate RR on the basis of a subset of significantly improve the process of
of available RR technologies, it is also breaths may be biased by respiratory pauses pneumonia diagnosis. New devices not only
important to address the value of RR as a or brief periods of tachypnea in healthy must be evaluated for their effectiveness in
diagnostic tool for pneumonia. Many factors newborns (35). In younger children, periods measuring RR in young children and infants
can influence RR, including temperature, of respiratory distress and fast breathing can but also should be designed specifically for
agitation, and whether the child is awake. be irregular and intermittent. With this in use in low-resource settings. This should
A 2017 systematic review assessing the mind, RR measurement tools should allow involve prioritizing the needs of healthcare
accuracy of clinical symptoms in identifying for an assessment over a period of time providers and understanding the constraints
children with radiographic pneumonia rather than at a single time point. The of using this technology in low-resource
found that among children with cough, challenge in this is finding a middle ground settings. Furthermore, the lack of a gold
fever, or both, tachypnea did not increase between a rapid device appropriate for standard or even a common reference
the likelihood of radiographic pneumonia health workers with limited time and a tool standard may impede the process of
(33). Although tachypnea may be a tool with a long enough window to capture developing and evaluating future RR
in the diagnosis of pneumonia, tachypnea variation and identify the peak RR. devices. By identifying existing RR counters
should be assessed in tandem with other There were also limitations to our and highlighting the gaps in current
clinical signs and symptoms (such as work landscape analysis and literature review, evaluation protocols, we hope to encourage
of breathing) and should not act as a stand- most significantly that our review may not researchers, developers, manufacturers, and
alone diagnostic criterion. include all RR counters in development. innovators to address the need for better
There are clear limitations of current Work on RR counting and monitoring ways to diagnose pneumonia and reduce
RR devices. Manual counter technologies technologies spans many disciplines that use childhood mortality in low-resource
do not eliminate reliance on the observer disparate methods and have different aims. settings. A single accurate measurement
or susceptibility to observer error and Studies that did not include an assessment of of RR alone is unlikely to provide a clear
distractions. Automated RR technologies accuracy against a reference standard and diagnosis of pneumonia, but, rather,
can be expensive and may not be feasible those that did not provide results among measurement will need to be repeated over
for low-resource settings. Contact-based spontaneously breathing children younger time and combined with other clinical signs
monitors may not be suitable for neonates than 5 years of age were excluded from this and symptoms interpreted by a trained
because of the fragility of their skin and may analysis. We also did not review the non-English frontline health worker. n

1126 American Journal of Respiratory and Critical Care Medicine Volume 197 Number 9 | May 1 2018
CONCISE CLINICAL REVIEW

Author disclosures are available with the text Acknowledgment: The authors thank Jaclyn device categories and Laura Lamberti for her
of this article at www.atsjournals.org. Delarosa for her assistance in developing the support on a previous draft of this manuscript.

References 18. Shah SA, Fleming S, Thompson M, Tarassenko L. Respiratory rate


estimation during triage of children in hospitals. J Med Eng Technol
1. World Health Organization. Fact sheet: pneumonia. 2016 [accessed 2015;39:514–524.
2017 Aug 18]. Available from: http://www.who.int/mediacentre/ 19. Kraaijenga JV, Hutten GJ, de Jongh FH, van Kaam AH. Transcutaneous
factsheets/fs331/en/. electromyography of the diaphragm: a cardio-respiratory monitor for
2. Rambaud-Althaus C, Althaus F, Genton B, D’Acremont V. Clinical preterm infants. Pediatr Pulmonol 2015;50:889–895.
features for diagnosis of pneumonia in children younger than 5 years: 20. van Gastel M, Stuijk S, de Haan G. Robust respiration detection from
a systematic review and meta-analysis. Lancet Infect Dis 2015;15: remote photoplethysmography. Biomed Opt Express 2016;7:
439–450. 4941–4957.
3. Nair H, Simões EA, Rudan I, Gessner BD, Azziz-Baumgartner E, Zhang 21. Seddon P, Sobowiec-Kouman S, Wertheim D. Infant home respiratory
JSF, et al.; Severe Acute Lower Respiratory Infections Working Group. monitoring using pulse oximetry. Arch Dis Child 2016; [online ahead
Global and regional burden of hospital admissions for severe acute of print] 7 Jul 2016; DOI: 10.1136/archdischild-2016-310712.
lower respiratory infections in young children in 2010: a systematic 22. Janssen R, Wang W, Moço A, de Haan G. Video-based respiration
analysis. Lancet 2013;381:1380–1390. monitoring with automatic region of interest detection. Physiol Meas
4. World Health Organization. Integrated management of childhood illness 2016;37:100–114.
chart booklet. Geneva: World Health Organization; 2014. 23. Al-Naji A, Chahl J. Remote respiratory monitoring system based on
5. Gadomski AM, Khallaf N, el Ansary S, Black RE. Assessment of developing motion magnification technique. Biomed Signal Proc
respiratory rate and chest indrawing in children with ARI by primary Control 2016;29:1–10.
care physicians in Egypt. Bull World Health Organ 1993;71:523–527. 24. Bang AT, Bang RA. Breath Counter: a new device for household
6. Noordam AC, Barberá Laı́nez Y, Sadruddin S, van Heck PM, Chono AO,
diagnosis of childhood pneumonia. Indian J Pediatr 1992;59:79–84.
Acaye GL, et al. The use of counting beads to improve the
25. Simoes EAF, Roark R, Berman S, Esler LL, Murphy J. Respiratory rate:
classification of fast breathing in low-resource settings: a multi-
measurement of variability over time and accuracy at different
country review. Health Policy Plan 2015;30:696–704.
7. Synovate Uganda. ARI timer research report for UNICEF: technical counting periods. Arch Dis Child 1991;66:1199–1203.
report. Kampala, Uganda: Synovate Uganda; 2011. 26. Bland JM, Altman DG. Statistical methods for assessing agreement
8. Lenahan JL, Ginsburg A. Towards a better diagnosis of childhood between two methods of clinical measurement. Lancet 1986;1:307–310.
pneumonia: a systematic review of tools to measure respiratory rate. 27. Severinghaus JW, Naifeh KH, Koh SO. Errors in 14 pulse oximeters
Presented at the 48th Union World Conference on Lung Health. during profound hypoxia. J Clin Monit 1989;5:72–81.
October 11–14, 2017, Guadalajara, Mexico. Abstract A-911-0011- 28. UNICEF. Target product profile: Acute Respiratory Infection Diagnostic
00681. Aid (ARIDA). Copenhagen: UNICEF Supply Division; 2014.
9. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred 29. Muro F, Mosha N, Hildenwall H, Mtei F, Harrison N, Schellenberg D,
reporting items for systematic reviews and meta-analyses: the et al. Variability of respiratory rate measurements in children
PRISMA statement. PLoS Med 2009;6:e1000097. suspected with non-severe pneumonia in north-east Tanzania. Trop
10. Johansson A, Oberg PA, Sedin G. Monitoring of heart and respiratory Med Int Health 2017;22:139–147.
rates in newborn infants using a new photoplethysmographic 30. Karlen W, Gan H, Chiu M, Dunsmuir D, Zhou G, Dumont GA, et al.
technique. J Clin Monit Comput 1999;15:461–467. Improving the accuracy and efficiency of respiratory rate
11. Olsson E, Ugnell H, Oberg PA, Sedin G. Photoplethysmography for measurements in children using mobile devices. PLoS One 2014;
simultaneous recording of heart and respiratory rates in newborn 9:e99266.
infants. Acta Paediatr 2000;89:853–861. 31. Spence H, Baker K, Wharton-Smith A, Mucunguzi A, Matata L, Habte T,
12. Neuman MR, Watson H, Mendenhall RS, Zoldak JT, Di Fiore JM, et al. Childhood pneumonia diagnostics: community health workers’
Peucker M, et al.; Collaborative Home Infant Monitor Evaluation and national stakeholders’ differing perspectives of new and existing
(CHIME) Study Group. Cardiopulmonary monitoring at home: the aids. Glob Health Action 2017;10:1290340.
CHIME monitor. Physiol Meas 2001;22:267–286. 32. UNICEF. Target product profile: Pneumonia acute respiratory infection
13. Roback K, Nelson N, Johansson A, Hass U, Strömberg T. A new
diagnostic aid - introduction. Copenhagen: UNICEF Supply Division; 2014.
fiberoptical respiratory rate monitor for the neonatal intensive care
33. Shah SN, Bachur RG, Simel DL, Neuman MI. Does this child have
unit. Pediatr Pulmonol 2005;39:120–126.
pneumonia?: The rational clinical examination systematic review.
14. Wertheim D, Olden C, Savage E, Seddon P. Extracting respiratory data
JAMA 2017;318:462–471.
from pulse oximeter plethysmogram traces in newborn infants. Arch
Dis Child Fetal Neonatal Ed 2009;94:F301–F303. 34. Al-Khalidi F, Saatchi R, Elphick H, Burke D. An evaluation of thermal
15. Wertheim D, Olden C, Symes L, Rabe H, Seddon P. Monitoring imaging based respiration rate monitoring in children. Am J Eng Appl
respiration in wheezy preschool children by pulse oximetry Sci 2011;4:586–597.
plethysmogram analysis. Med Biol Eng Comput 2013;51:965–970. 35. Brooks LJ, DiFiore JM, Martin RJ; Collaborative Home Infant
16. Petrus NC, Thamrin C, Fuchs O, Frey U. Accuracy of tidal breathing Monitoring Evaluation. Assessment of tidal volume over time in
measurement of FloRight compared to an ultrasonic flowmeter in preterm infants using respiratory inductance plethysmography, the
infants. Pediatr Pulmonol 2015;50:380–388. CHIME Study Group. Pediatr Pulmonol 1997;23:429–433.
17. Kohn S, Waisman D, Pesin J, Faingersh A, Klotzman IC, Levy C, et al. 36. McDonagh M, Peterson K, Parminder R, Chang S, Shekelle P. Avoiding
Monitoring the respiratory rate by miniature motion sensors in bias in selecting studies. In: Methods guide for comparative
premature infants: a comparative study. J Perinatol 2016;36: effectiveness reviews. Rockville, MD: Agency for Healthcare
116–120. Research and Quality; 2012.

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