Article

Thermal imaging applications in neonatal care: a scoping review

Topalidou, Anastasia, Ali, Nazmin, Sekulic, Slobodan and Downe, Soo

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Topalidou, Anastasia ORCID: 0000-0003-0280-6801, Ali, Nazmin, Sekulic, Slobodan and Downe, Soo ORCID: 0000-0003-2848-2550 (2019) Thermal imaging applications in neonatal care: a scoping review. BMC Pregnancy and Childbirth, 19 (1). pp. 1-14.

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RESEARCH ARTICLE Open Access

Thermal imaging applications in neonatalcare: a scoping reviewAnastasia Topalidou1* , Nazmin Ali1, Slobodan Sekulic2 and Soo Downe1

Abstract

Background: In neonatal care, assessment of the temperature of the neonate is essential to confirm on-goinghealth, and as an early signal of potential pathology. However, some methods of temperature assessment involvedisturbing the baby, disrupting essential sleep patterns, and interrupting maternal/infant interaction. Thermalimaging is a completely non-invasive and non-contact method of assessing emitted temperature, but it is not astandard method for neonatal thermal monitoring. To examine the potential utility of using thermal imaging inneonatal care, we conducted a comprehensive systematic scoping review of thermal imaging applications in thiscontext.

Methods: We searched EMBASE, MEDLINE and MIDIRS.

Results: From 442 hits, 21 met the inclusion criteria and were included in the review. A significant number (n = 9)were published in the last 8 years. All the studies were observational studies, with 20 out of 21 undertaken in NorthAmerica or Europe. Most of them had small cohorts (range 4–29 participants). The findings were analysed narratively,to establish the issues identified in the included studies. Five broad themes emerged for future examination. Thesewere: general thermal physiology; heat loss and respiratory monitoring; identification of internal pathologies, includingnecrotising enterocolitis; other uses of thermal imaging; and technical concerns. The findings suggest that thermalimaging is a reliable and non-invasive method for continuous monitoring of the emitted temperature of the neonates,with potential for contributing to the assurance of wellbeing, and to the diagnosis of pathologies, including internalabnormalities. However, the introduction of thermal imaging into everyday neonatology practice has severalmethodological challenges, including environmental parameters, especially when infants are placed in incubatorsor open radiant warmers.

Conclusion: In conclusion, although the first attempt at using thermal imaging in neonatal care started in theearly-1970s, with promising results, and subsequent small cohort studies have recently reinforced this potential,there have not been any large prospective studies in this area that examine both the benefits and the barriers toits use in practice.

Keywords: Thermal imaging, Infrared thermography, Neonatology, Newborn, Monitoring, Temperature

BackgroundAssessment of the neonatal temperature is important,because normothermia offers reassurance of continuedwellbeing, and because both hyperthermia and hyper-thermia are associated with underlying conditions thatcan result in long term irreversible damage, and evendeath. The issue of neonatal temperature assessment has

increased in prominence recently, as concern about sep-sis in neonates (both term and preterm) has highlightedthe lack of knowledge around hypothermia as a markerof advanced infection [1–6]. The optimum means of en-suring a stable neonatal temperature for a healthy neo-nate in the first hours of life is to ensure the newbornstays in skin-to-skin contact with the mother, as thephysiological maternal response is to thermoregulatewith the baby [1–3]. However, for sick term neonates, orfor those born preterm, where staying with the motheris not an option, regular assessment of temperature is an

© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, andreproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link tothe Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

* Correspondence: atopalidou@uclan.ac.uk1Research in Childbirth and Health Unit, School of Community Health andMidwifery, Faculty of Health and Wellbeing, University of Central Lancashire,Preston, UKFull list of author information is available at the end of the article

Topalidou et al. BMC Pregnancy and Childbirth (2019) 19:381 https://doi.org/10.1186/s12884-019-2533-y

essential part of good quality care. Some of the currentmeans of assessing neonatal temperature can disturb theusual sleep/wake patterns of sick neonates, and can evenbe invasive and distressing [7]. This paper examinescurrent evidence relating to the potential for thermal im-aging as an accurate and non-invasive method of con-tinuously assessing neonatal temperature under thesecircumstances.

Physiology of fetal and neonatal thermoregulationThe fetal temperature is linked to maternal temperatureand to the maternal-fetal thermal gradient. Within theutero-environment, fetal thermoregulation is dependenton the mother, as heat is transferred to the fetus via theplacenta and the uterus. In addition, the heat that isgenerated by the fetus, as a by-product of its metabol-ism, is eliminated through the mother. The fetal heatproduction and loss to its maternal surroundings resultsin thermal stability, with the fetus maintaining atemperature that is 0.3 °C to 0.5 °C higher than that ofthe mother [1–4].However, directly after birth, there is a decline in

temperature. This is mostly due to the fact that the new-born is exposed to a new environment and has a lack ofinsulation [2, 8]. Thus, to increase body temperature andprevent heat loss, non-shivering thermogenesis (NST)must occur for the newborn to survive [4, 8]. If NST isinsufficient, this poses a risk of the infant developinghypothermia (body temperature below 36.5 °C). This canresult in physiological changes occurring within the in-fant, such as vasoconstriction. Premature newborns areat a greater risk of developing hypothermia, because theyhave a lower percentage of brown fat in comparison tofull-term newborns, since brown fat is acquired in laterweeks of gestation [3, 9].

The case for temperature measurement with thermalimagingSeveral new measuring techniques to assess temperatureover an extended period have been introduced in the lastdecade. Some of them involve the use of probes and sen-sors that require contact which may cause discomfort(especially for the sensitive skin of preterm babies) andmechanical stress, as well as posing possible hygienerisks [7, 10]. Therefore, contact-free and non-invasivetechniques are more desirable. One such a technique isthermal imaging (TI) (infrared thermography). TI relieson the infrared radiation that is emitted from the humanbody. The amount of the radiation that is emitted by anyobject depends on the temperature of the object and itsemissivity [11]. The human body has an emissivity of0.98 making it almost a perfect emitter [12]. Addition-ally, the higher the temperature, the more radiation isemitted [11]. The actual exitant radiation from an object

or body is described by the emitted, the radiated and thetransmitted radiation, the sum of which is always one.Knowing that the human skin is not transmissive butopaque the exitant radiation consists of emitted andreflected radiation [13]. A TI device (camera) can cap-ture images (thermograms) that show thermal distribu-tions of the epidermis in real-time [8, 14]. A thermalimage of a human body is a visual representation of thesurface skin temperature. However, human skin is achallenging “material”, as the emitted radiation may add-itionally represent heat transferred from within thebody-core structures, as veins, organs, or lumps and in-flammations [10, 12, 15, 16]. In newborns, this can be anadvantage, however, as TI has the additional ability to ef-ficiently record the thermal energy (heat in transfer)from highly vascular systems, such as heart and liver, byrepresenting warmer areas on the surface, due to thethinner skin and poor insulation [15]. Several re-searchers have used TI to investigate the body surfacetemperature, the energy loss and other factors related toneonatal thermoregulation [15, 17–19].The aim of the current scoping review was to provide

a comprehensive overview of the literature regarding theapplication of TI in neonatal care and outcomes associ-ated with the use of this method, along with an identifi-cation of the remaining knowledge gaps.

MethodsScoping reviews have been increasingly prevalent in theliterature over the last decade or so. Mayes et al. (2001)[20] state that such a review usually: “aims to map rap-idly the key concepts underpinning a research area andthe main sources and types of evidence available, andcan be undertaken as stand-alone project in their ownright, especially where an area is complex or has not beenreviewed comprehensively before”. The methodology canvary, including both qualitative and quantitative re-search, and it is more iterative and flexible than thatstandard meta-analytic systematic review approaches. Itis usually used either to identify research gaps, or toprovide a narrative summary of the field under scrutiny[21, 22]. The protocol for the current review was struc-tured using the scoping review methodological frame-work described by Arksey and O’Malley (2005) [22].

Search strategyAn extensive literature search to identify studies pub-lished from the earliest date in each database untilAugust 2017 was conducted. Two authors performed asearch of the following international databases: EMBASE(1974 to 1st August 2017), MEDLINE (1946 to August2017 week 1) and Maternity & Infant Care Database –MIDIRS (1971 to July 2017). In order to find all the re-lated articles, we used sensitive search strategies to

Topalidou et al. BMC Pregnancy and Childbirth (2019) 19:381 Page 2 of 14

reduce the risk of losing any articles. The search was de-signed to retrieve all articles combining the concepts of“thermography”, or “thermographic”, or “thermal im-aging”, or “long-infrared” and “infant”, or “newborn”, or“neonatal”, or “neonate”. The search strategy was limitedto the English language only. The above sources and da-tabases were considered by the researchers as the mostsuitable for the objective of the study, as we thoughtthey would include the majority of published papers inthe general field of interest.

Inclusion/exclusion criteriaWe did not assess the methodological quality of the in-cluded studies in this scoping review, as the purpose wasto scan the literature and to determine what has beenreported and what needs further investigation. All re-search studies reporting the use of TI in newborns wereincluded. We used the World Health Organisation(WHO) definition of ‘newborn’ [23]: “A newborn infant,or neonate is a child under 28 days of age”.Publications presenting studies of newborns older than

28 days, or where the age was not specified, were ex-cluded. Papers that were not available in full text, thatwere not focused on healthcare, and that did not reporta research or case study with clearly defined methodsand results, were also excluded.

Screening and chartingDuplicate articles were automatically identified by thesearch tool and removed from the database prior toscreening. A two-step process with two independent re-viewers for each step were performed. At the first stage,the titles and abstracts of articles identified by the searchstrategy were screened according to the inclusion andexclusion criteria described above. Disagreement be-tween reviewers during this screen resulted in the arti-cle’s inclusion for full-text review.Studies meeting the criteria outlined were charted

using Microsoft Excel and screened further as full manu-script. The full texts were assessed, at this stage, for finalinclusion in our study. When the final number of the re-cords selected to be included in the current study wereidentified, an additional check was performed on thebibliographic reference lists of these articles, to identifyany additional eligible publication.

AnalysisA narrative analytic approach was taken, based on keyprinciples from meta-synthesis theory [24]. First, two au-thors independently read four of the included papers,and charted the themes they observed. These were thenagreed by consensus. The rest of the data set were thenread by the same two authors independently and thedata were mapped to the initial themes. Any data that

could not be mapped to these themes were coded intonew themes, and the process continued iteratively. Thefinal thematic structure was agreed between all theauthors.

ResultsA total of 442 records were identified by the searchstrategy of the databases (EMBASE, MEDLINE andMIDIRS). After de-duplication 295 records werescreened by title in order to make the procedure moremanageable. Overall, 137 records were screened by ab-stract, and 68 were taken forward for full text review.After the final full-text selection, 19 records remained andwere included in this review. In two of these [25, 26] theage of the neonates was not explicitly defined as a number,but the text indicated that they were eligible, and so theywere included. Checking the references of included papersresulted in two additional included studies. The screeningprocess and final included studies are documented in theflow diagram (Fig. 1).The characteristics of the 21 included studies are pre-

sented in. All were observational studies. The twentyone of them were case series and one was a comparativecohort study. Although the first attempts to use TI inneonatology started in the early-1970s, two chrono-logical gaps, with no papers published, were observed.The first gap was between 1980 and 1997 and the sec-ond one between 2003 and 2008, after which interestseems to be rapidly rising. The number of publicationsper decade are presented in Fig. 2.The included studies were undertaken in the following

countries: USA (n = 9 studies), Austria (n = 3), Germany(n = 2), France (n = 1), Sweden (n = 1), Finland (n = 1),Sweden and Finland (n = 1), Japan (n = 1) England (n =1), and Canada (n = 1). They generally included smallsamples, ranging from n = 4 infants [35], to n = 29 pre-term neonates assessed on night 9 of life [39]. Although,there were two studies with larger cohorts of 41 [17]and 43 newborns [29], both of them had their cohortsdivided into 4 smaller sub-groups with different charac-teristics. Some studies included larger cohorts [15, 25],but it was not clear how many of the assessed newbornswere < 28 days of age (Table 1).The techniques and cameras used progressed rapidly

through the years. The early studies [27–29, 31] usedthe very first commercial infrared system named AGAThermovision (by AGA, Lidingo, Sweden), which wasavailable on the market before the mid-1960’s. Modelssuch as the 660 and 661 had a single element liquidnitrogen-cooled indium antimonide (InSb LN2) detector,and field of view (FOV) 5ox5o, with the camera aloneweighing 25 kg. The total weight of the whole thermo-graphic system was about 75 kg [40]. In 1980, Clark andStothers [14] used the AGA Thermovision 680 that was

Topalidou et al. BMC Pregnancy and Childbirth (2019) 19:381 Page 3 of 14

Fig. 1 Flow chart of literature review process

Fig. 2 The number of publications per decade

Topalidou et al. BMC Pregnancy and Childbirth (2019) 19:381 Page 4 of 14

Table

1Finalrecords

includ

edin

thescop

ingreview

basedon

theinclusionandexclusioncriteria

(inchrono

logicalo

rder)

Autho

r(s)

Year

Type

ofStud

yCou

ntry

Purposeof

theStud

yPo

pulatio

nTIAssessm

entTool

Viitane

n&Kivikoski[27]

1971

Caseseries

Finland

Toassess

thethermog

raph

icalchange

sin

thetempe

rature

ofthene

wbo

rnsandthe

comparison

with

localskintempe

rature

measuremen

ts.

18ne

wbo

rns(im

med

iatelyafterde

livery)

AGAThermovisionsystem

Mod

el652

Tahtietal.[28]

1972

Caseseries

Finland&

Swed

enTo

record

theem

itted

heat

ofwideareas

ofinfant’sbo

dyandto

stud

ytheinfant’s

firstreactio

nto

acold

environm

ent.

16infantsdirectlyafterde

livery(12he

althy

full-term

infantsof

norm

alweigh

t;2he

althy

prem

atureinfantswith

1800

gand2200

gbo

dyweigh

t;and2asph

yxiatedbabies

with

1800

gand2600

gbirthweigh

t)

AGAThermovisionsystem

Mod

el661

Ryland

eret

al.[29]

1972

Caseseries

(with

4grou

ps)

Swed

enTo

demon

strate

ifacold-in

ducedincrease

inhe

atradiationappe

ared

over

areas

whe

rebrow

nfatshou

ldbe

subcutaneo

usly

situated

.

43he

althyinfants(gestatio

nalage

38–44weeks)

checkedbe

fore

thetenthdayof

life

Group

1,n=19:infantswith

abirthweigh

tof

2750

gto

3820

g(in

environm

ental

tempe

rature

of24

°C)

Group

2,n=10:infantswith

abirthweigh

tof

3240

gto

4020

g(placedin

anincubator)

Group

3,n=7:infantswith

abirthweigh

tof

1860

gto

2680

g(treated

inthesameway

asGroup

2)Group

4,n=7:infantswith

abirthweigh

tof

2980

gto

4370

g(in

awater

bath

of38

°C)

AGAThermovisionsystem

Mod

el660

Perlstein

etal.[30]

1972

Caseseries

USA

Toinvestigateifinfant

ageisan

impo

rtant

variableto

consider

inevaluatin

ginterscapu

larskin

tempe

raturesin

cold-stressedbabies.

14full-term

andprem

atureinfants(7

ofthe

infantswereless

than

24hand7morethan

5days

oldat

thetim

eof

exam

ination)

Nobrandname(the

rmog

raph

ysystem

Barnes

Engine

eringCo,with

anIndium

Antim

onite

sensor

2–4.4μm

.4thermog

ramspe

rsecond

)

Bhatiaet

al.[31]

1976

Com

parative

coho

rtstud

y(fo

llow

upof

patients’grou

psub-sample)

USA

ToinvestigateifTIcanbe

inform

ativein

acuteandchronicliver

disease,particularly

onfollow-upbasis.

Patientsgrou

p:62

infantsandchildren

from

3weeks

to17

yearsof

age

Con

trol

Group

:32he

althychildrenfro

m2days

to8yearsof

age

(nospecificatio

non

how

manyof

them

werene

wbo

rns<28

days

ofage)

Follow-upwas

perfo

rmed

in28

ofthe

62participants(patientsgrou

p)

AGAThermovisionsystem

(nomod

elde

scrip

tion)

Pomerance

etal.[15]

1977

Caseseries

USA

Tode

term

ineno

rmalanterio

randpo

sterior

thermog

ramsof

thetrun

kof

ane

wbo

rn;

andto

investigatewhe

ther

deep

-lying

organs

canbe

detected

atthesurface.

37ne

wbo

rns(age

rang

eno

tspecified

for

who

legrou

p).The

rewas

one2-day-old

term

,one

3-days

oldterm

,one

18days

oldpre-term

,one

19days

oldpre-term

etc.

Spectrothe

rm2000

Thermog

raph

icSystem

Clark

&Stothe

rs[14]

1980

Caseseries

England

Tovisualiseskin

tempe

rature

distrib

utions

inne

wbo

rns;andto

compare

tempe

ratures

obtained

from

thermog

rams(the

rmal

camera)

toskin

tempe

raturesmeasured

with

athermom

eter.

17ne

wbo

rns4–13

days

old(15

were

full-term

and2werepreterm).

AGAThermovisionsystem

Mod

el680

Oya

etal.[32]

1997

Caseseries

Japan

Tomeasure

theextent

ofno

n-shivering

thermog

enesis(NST)in

brow

nadipose

tissueof

human

newbo

rnsreceiving

routinethermalcare

andto

exam

inethe

influen

ceof

oxygen

levelsat

birthon

the

15he

althyfull-term

newbo

rns

(five

minutes

afterbirth)

ThermalVide

oSystem

3000

ME,Japan

Avion

icsCo.

Topalidou et al. BMC Pregnancy and Childbirth (2019) 19:381 Page 5 of 14

Table

1Finalrecords

includ

edin

thescop

ingreview

basedon

theinclusionandexclusioncriteria

(inchrono

logicalo

rder)(Con

tinued)

Autho

r(s)

Year

Type

ofStud

yCou

ntry

Purposeof

theStud

yPo

pulatio

nTIAssessm

entTool

initiationof

NST.

Eket

al.[18]

1999

Caseseries

USA

Toinvestigatethechange

sin

heat

loss

whe

nradiantwarmerswereremoved

and

returned

toprem

atureinfants.

10prem

atureinfants(gestatio

nal

age31.4±5.5weeks),age

15±11.7days

600Linfraredim

agingradiom

eter

(Inframetrics)

Adamset

al.[19]

2000

Caseseries

USA

Totestane

wmetho

d–infrared

thermog

raph

iccalorim

etry

–against

respiratory

indirect

calorim

etry

tomeasure

meanbo

dytempe

rature

andcalculate

heat

loss.

10preterm

infants(34±23

days)

Inframetricsmod

el525infraredcamera

Christid

isIetal.[17]

2003

Caseseries

(with

4grou

ps)

Austria

Toinvestigateasurface

tempe

rature

profile

inne

wbo

rnswith

inthefirstho

urafterde

livery.

41ne

wbo

rns(with

inthefirstho

urafterbirth)

Group

1,n=19:infantsafterno

rmal

preg

nancy,

wrapp

edinto

cotton

immed

iately

afterde

livery

Group

2,n=15:infantsexam

ined

bypaed

iatricianun

deraradianthe

ater

Group

3,n=4:infantsafterno

rmal

preg

nancywho

hadskin-to-skin

contact.

Group

4,n=3:infantsafterno

rmal

preg

nancy,recorded

before

any

interven

tion.

ThermotracerTH

3100

(NEC

San-ei

Instrumen

ts,Japan)

Saxena

&Willital[26]

2008

Caseseries

Austria

Toassess

theapplicationof

TIto

iden

tify

patholog

iesin

1weekto

16year

oldchildren.

(Inne

wbo

rnswith

abdo

minalwalld

efect)

285patients;18

newbo

rns(>

1weekold)

Talytherm

thermalim

ager

(RankTaylor

Hob

sonLtd)

Rice

etal.[33]

2010

Caseseries

USA

Tomeasure

theabdo

minalsurface

tempe

rature

inlow

birthweigh

tne

wbo

rns,

usingthermog

raph

y,anddraw

ing

comparison

sbe

tweenabdo

minaland

thoracicsurface

tempe

raturesin

newbo

rns

with

andwith

outne

crotisingen

terocolitis

(NEC

).

13ne

wbo

rns;10

newbo

rnshad

radiog

raph

sandwereused

forcomparison

.(23–29

gestationalw

eeks;examined

durin

gthefirstmon

thof

life)

FLIR

SC640camera

Herry

etal.[25]

2011

Caseseries

Canada

Tocompare

thermog

ramsof

theabdo

men

ofhe

althyne

wbo

rnsandne

wbo

rnswith

NEC

,todistingu

ishdifferences

andto

investigateifTIissuitablefordiagno

sing

NEC

ininfants.

59ne

wbo

rns(48werehadage

stational

ageof

28.3±2.4weeks;11wereof

26.7±1.8weeks)

Nobrandname(Infraredcamera,

uncooled

microbo

lometer

focalp

lane

array,320×420pixels,the

rmaland

spatialsen

sitivity

of0.05°at

30°C

and

1.3mrad)

Abb

aset

al.[34]

2011

Caseseries

Germany

TouseTIto

mon

itorthermaldistrib

utions

ofne

onates

with

inthene

onatalintensive

care

unit.

7preterm

newbo

rns(gestatio

nalage

was

ameanof

29weeks,include

din

thestud

ydirectlyafterbirth)

Vario

CAM

hr.headcamera(InfraTech

GmbH

)

Knob

elet

al.[8]

2011

Caseseries

USA

Tomeasure

body

tempe

rature

ininfants

andexam

inetherelatio

nshipbe

tween

body

tempe

rature

andsymptom

sof

NEC

ininfantswith

low

birthweigh

ts.

10low

birthne

wbo

rns(gestatio

nalage

less

than

29weeks,examined

durin

gthefirst

5days

oflife)

FLIR

SC640un

cooled

infraredcamera

Knob

elet

al.[35]

2013

Caseseries

USA

Totestinstrumen

tatio

nandde

velop

4ne

wbo

rns,4hof

birth(<

29weeks

Not

men

tione

d

Topalidou et al. BMC Pregnancy and Childbirth (2019) 19:381 Page 6 of 14

Table

1Finalrecords

includ

edin

thescop

ingreview

basedon

theinclusionandexclusioncriteria

(inchrono

logicalo

rder)(Con

tinued)

Autho

r(s)

Year

Type

ofStud

yCou

ntry

Purposeof

theStud

yPo

pulatio

nTIAssessm

entTool

analyticmod

elsto

usein

alarger

stud

yto

exam

inede

velopm

entaltrajectoriesof

body

tempe

rature

andpe

riphe

ralp

erfusion

from

birthin

extrem

elylow

birthweigh

t(EBLW)infants.

gestationalage

)

Heimannet

al.[36]

2013

Caseseries

Germany

Toevaluate

skin

tempe

rature

byusing

different

positio

nswith

TIin

multip

lebo

dyareasof

preterm

infantsforde

tailed

inform

ationabou

ttempe

rature

regu

latio

nanddistrib

ution.

10preterm

infants(12–62

days

old)

Vario

Cam

hr-Head(InfraTecGmbH

,Germany)

Kurath-Kolleret

al.[37]

2015

Caseseries

Austria

Toevaluate

thesafety

oflaseracup

uncture

inne

wbo

rninfantsby

usingathermal

camerato

analysechange

sin

thermal

distrib

utions.

20ne

wbo

rns(23days

old)

FLIR

i5camera

Knob

el-Dailetal.[38]

2017

Caseseries

USA

Toexploretheutility

ofTIas

ano

n-invasive

metho

dformeasurin

gbo

dytempe

rature

inprem

atureinfantsin

anattempt

toregion

allyexam

inedifferentialtem

peratures.

Datawas

collected

from

31infantsoriginally;

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utilised for medical applications. Although it was lighterthan the earlier models (15 kg), due to its size andweight it was usually operated on a tripod. Other earlystudies (1977) used the Spectrotherm 2000 by GeneralElectric, which was equipped with a single elementliquid nitrogen cooled Mercury Cadmium Telluride(HgCdTe) detector, with a resolution of 256 × 256points, and the need for conversion and use of a Polar-oid film [15]. The latest studies used the much more so-phisticated high resolution radiometric thermal imagers,such as the FLIR SC640 uncooled camera (1.8 kg) withthermal sensitivity of <30mK, resolution of 640X480,FOV ranging from 12°× 9° to 45°× 34° and radiometricvideo recording with real-time analysis (2017) [38].The areas of interest that have been investigated to

date with these technologies are presented in Table 2.The narrative analysis generated five broad themes:

general thermal physiology; heat loss and respiratorymonitoring; identification of internal pathologies; otheruses of TI; and technical concerns.

General thermal physiologySince the beginning of 1970’s researchers used thermog-raphy as a method to map out the heat distribution ofthe skin. In 1971, a study assessing the skin circulationchanges in newborns, showed differences in the thermalpatterns and the level of temperature rise between thetrunk and the colder limbs. These patterns were notconstant in infants whose mother had pre-eclampsia incomparison with those who did not even though all thebirths were vaginal in this cohort. In addition, this studyshowed that thermograms and skin temperature curvesboth recorded similar data for changes in postnataltemperature [27].Continuous recording of heat emission of wide areas

of the newborn, was reported by the Tahti et al. [28]. Inthe same study, the temperature change of the umbilical

cord was recorded, showing that the temperature of theumbilical cord dropped instantly in infants born withnuchal cord but took 30–60 s for infants born withoutnuchal cord. Rylander et al. [29] recorded the dorsalsurface of infants during 30 min of exposure to an ambi-ent temperature (21-23 °C), reporting no relation to thecondition/treatment before exposure and no significantdifferences between the four observational groups(Table 1). In another study, the age-related thermaladaptive phenomenon in infants was described, follow-ing the recording of the interscapular area, whichshowed that temperature was maintained even undercold-stress conditions [30].In 1977 Pomerance et al. [15] conducted a study using

TI to determine the typical anterior and posterior viewsof the trunk of a newborn. Over three months, anteriorand posterior thermograms of 37 newborns were re-corded. Results demonstrated that the heart, liver andkidneys were warm areas due to being highly vascularorgans. Warm areas were also observed in the neck, nearthe umbilical and areas that have high percentages ofbrown fat. An infant who developed congestive heartfailure demonstrated a cooler chest area. A thermogramof another infant revealed a warm area over the leftkidney – but not over the right, suggesting limited bloodsupply to the right kidney. This was later confirmedthrough autopsy. This study proved that TI has manypotential uses within neonatal care and can be used toscreen newborns for internal abnormalities, as deep-lying structures in newborns have less insulation.Three years later, in 1980, Clark and Stothers [14] ana-

lysed temperature distributions of infants in different en-vironmental conditions ranging from 28.5 °C to 32 °C.Infrared colour thermography was used to determine theskin temperature of seven infants. In addition, multiplerecordings of skin temperature, using an Ellab UniversalThermometer with a probe, were then taken from twelve

Table 2 Summary of the regions of interest that were assessed up to date

Regions of interest/investigation Authors - Studies

Body surface (skin) temperature, and temperaturedistributions (patterns): Forehead, nose, cheeks,chin, earlobe, nape, interscapular area, hand, foot,upper trunk, buttock, thigh, calf, arm, abdomen, back.

Viitanen&Kivikoski (1971); Tahti et al. (1972); Rylander et al. (1972);Perlstein et al. (1972); Bhatia et al. (1976); Pomerance et al. (1977);Clark &Stothers (1980); Ek et al. (1999); Oya et al. (1997);Adams et al. (2000); Christidis et al. (2002); Saxena&Willital (2008);Rice et al. (2010); Herry et al. (2011); Knobel et al. (2011); Abbas et al. (2011);Knobel et al. (2013); Kurath-Koller et al. (2015); Knobel-Dail et al. (2017);Barcat et al. (2017)

Deep structures/organs: heart, liver and kidneys. Bhatia et al. (1976); Pomerance et al. (1977)

Clinical states: Pathologies, abdominal wall defects,NEC, heart failure, liver diseases, kidney dysfunction.

Bhatia et al. (1976; Pomerance et al. (1977); Saxena&Willital (2008);Rice et al. (2010); Herry et al. (2011); Knobel et al. (2011)

Heat loss Tahti et al. (1972); Ek et al. (1999); Adams et al. (2000)

Respiratory monitoring Adams et al. (2000); Abbas et al. (2011)

Safety of laser acupuncture Kurath-Koller et al. (2015)

Sleep propensity Barcat L et al. (2017)

Topalidou et al. BMC Pregnancy and Childbirth (2019) 19:381 Page 8 of 14

infants. They observed that, within a warmer environ-ment, the upper anterior region of the neonatal trunk wasat a higher temperature in comparison to the posteriorregion. It was also observed that there was a decrease intemperature in the extremities. In cooler conditions, hotspots were identified over the jugular vein and regions ofthe carotid artery.Almost 20 years later, Oya et al. [32], used TI to assess

the extent of NST in brown adipose tissue of infantsreceiving routine care. The findings of this study camein line with earlier findings [29, 30] showing that theinterscapular area was warmer than other parts of thebody and that NST is activated soon after birth, provingthat TI could be useful for the detection of NST in sub-cutaneous brown adipose tissue.Another area of research has been skin-to-skin care

(SSC) in premature newborns. Knowing the variouspositive effects of SSC, in 2012 TI was used to assessthe skin temperature, distribution and kinetics, to clarifytemperature regulation longitudinally. Results showed thatduring SSC premature newborn’s average skin temperatureincreased and then dropped down after placing back intothe incubator, to a level that was significantly lower, com-pared to the initial recording. Premature infants neededmore that 10min to regulate their temperature back to theoriginal level. As daily routine care is performed directlyafter the infants’ placement into the incubator, the abovefinding is of clinical significance [36].

Heat loss and respiratory monitoringThe first attempt to record heat loss and infant’s reac-tion to a cold environment was made by Tahti et al., in1972 [28]. By using an early model of an infrared camerain combination with an electrical thermometer, theauthors found that premature infants showed fairly uni-form and similar patterns of change in heat emission asfull-term infants. A quick drop of temperature startingfrom the periphery and rapidly advancing in centripetaldirection was observed. During delivery, once the fetalface appeared, its temperature decreased by 2 °C within10 s. Also, the skin temperature of the anterior thoracicarea dropped instantaneously with the first deep breath.On the other hand, asphyxiated babies showed a differ-ent pattern, with the temperature of the face, handsand legs dropping, but the temperature of the trunkremaining warm, until the establishment of the respir-ation. Almost three decades later, in another study,assessing the body surface temperature profiles in fourgroups of infants within an hour after birth, the authorsreported similar patterns of heat change, with the per-ipheral sites becoming cooler more quickly, in contrastwith the trunk. In addition, the author reported thatskin-to-skin contact is an effective method to preventheat loss [17].

Ek et al. [18] studied 10 premature infants to observewhat changes would occur when they were removedfrom radiant warmers. Infrared thermographic calorimetrywas used. This method is a combination of a thermal cam-era and equations that calculate heat expenditure. Usingcomputer software, mean body surface temperatures(MBST) were calculated. They observed that once theradiant warmer was removed, there was a large increase inheat loss and MBST decreased. It was also found thatthere was a correlation between temperature and age, asthe youngest newborns had greater declines in MBST anda larger increase in heat loss. Similarly, a year later, Adamset al. [19] conducted a study using infrared thermographiccalorimetry to examine energy loss in 10 preterm infants.Respiratory indirect calorimetry was also used to drawcomparisons. Both methods were used to determine themean of the infants’ body surface temperature. Resultsshowed that there was no significant difference betweenthe mean values obtained from both methods. Theauthors concluded that the use of TI to calculate energyloss was promising. In another study, real-time TI record-ing was used to monitor rate of respiration in seven pre-mature neonates (2 in warmer beds and 5 in incubators)and similar results were obtained. Specifically, there weretemperature changes within the nasal area (the maximumchange being 0.66 °C) indicating that TI could be used inintensive care units to monitor respiration and heat loss ofneonates [34].

Identification of internal pathologies (particularly,necrotising enterocolitis)TI appears to aid in the diagnosis of pathologies in neo-natal internal organs. The first report was published in1976. In this study, researchers investigated the applica-tion of TI in the study of liver diseases. The resultsshowed that specific patterns of heat emission over theliver area were predominant in the participants who hada hepatic disease, such as neonatal hepatitis. Althoughthe findings were not helpful in differential diagnosis be-tween the different liver diseases and conditions, the au-thors stated that TI could be useful in follow-upinvestigations, due to its ability to identify changes inthermal patterns [31]. In addition, as presented above,Pomerance et al. [15], demonstrated that pathologies ofhighly vascular internal organs, as heart and kidneymight be detectable by TI.In 2008, Saxena and Willital [26] conducted a study

that evaluated the application of TI to diagnose patholo-gies in children aged 1 week to 16 years old. Participantsincluded 18 neonates with abdominal wall defects (gas-troschisis or omphalocele). Due to the open abdomensolvent-dried dura implants were applied. During thefirst week the area that was covered with the patch pre-sented lower temperatures in comparison with the skin

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of the abdominal wall. Four weeks after implantationand until complete implant integration the temperatureof the patches increased, appearing higher than the abdo-men’s skin, demonstrating the vascular proliferation andthe patch integration. The same participants were followed-up a year later showing no significant temperature differ-ences on their abdominal wall.Herry et al. (2011) [25] studied 48 healthy newborns

and 11 newborns diagnosed with necrotising enterocoli-tis (NEC) to distinguish thermographic differences thatwould aid in the diagnosis of NEC in future. The surfacetemperatures of different areas of the abdomen weremeasured using a thermal camera at a distance of 60 cm.It was found that over a period of time there was a gen-eral decrease in temperature in both groups. However,the NEC group had a lower decrease in comparison tothe healthy group, possibly due to the increased amountof heat emitted from inflamed bowels. This finding sug-gests that NEC newborns can be differentiated fromhealthy newborns, and that TI can aid in the diagnosisof NEC.This finding is reinforced with a study assessing the

use of TI in low birth weight newborns to measure ab-dominal skin temperature and to assess the relationshipbetween abdominal skin temperature and NEC [33]. Intotal, 10 infants aged 23 to 29 gestational weeks (of 13in the cohort) were examined to assess the correlationbetween temperature and NEC. These infants had boththermograms and radiographs of the abdomen. Tem-peratures of the abdomen and thorax were measured,and means were calculated. Axillary temperatures werealso taken by a probe to measure the accuracy of TI.Those that had been diagnosed with NEC had lowerabdominal temperatures in contrast to neonateswithout NEC [33]. Similar results were also found byKnobel et al. (2011) [8]. They conducted two pilot stud-ies: one studied the feasibility and the methods of usingTI to record the body temperatures of neonates in in-cubators during their first 5 days of life, and the otherexamined the correlation between body temperaturesof 10 extremely low birth weight neonates and thepossible development of NEC. Infants were held in thesupine position whilst the thermal camera was used.Mean temperatures of the abdomen and thorax werecalculated to determine if there was an association withNEC. In the 10 premature neonates, it was observedthat those with a diagnosis of NEC (n = 10) had lowerabdominal temperatures, agreeing with the results fromRice et al. 2010 [33] and Herry et al. 2011 [25]. Further-more, the pilot studies confirmed that TI is a safe andcompletely non-invasive method to be used on prema-ture infants with low birth weights, while being able tobe used for continuous daily imaging and temperaturerecording.

Some years later, Knobel-Dail et al. (2017) [38] investi-gated the accuracy of TI in comparison to using a probeto measure body temperature, and the possibility ofusing TI to detect early perfusion injury signs, such asNEC in premature neonates. Temperatures of the abdo-men and foot were measured using probes, while a ther-mal camera was used to take images of the neonateswithin their first five days of life. Thermograms were ob-tained from 22 infants; the first two infants were usedfor training research assistants in TI. It was found thatmean temperature of the abdomen was 36.44 °C whenusing a probe, whilst it was recorded to be 36.57 °Cusing TI showing a good level of agreement. Agreementof the mean temperatures of the foot measured by thetwo methods was not as good. However, the mean dif-ference was still centred around 0. This demonstratesthat TI has potential in aiding in diagnosing and caringfor newborns with NEC.

Other uses of thermal imagingTI has been used to assess the relationship between skintemperatures, vasodilation and sleep propensity in pre-mature newborns. In a study conducted by Barcat et al.(2017) [39] twenty nine premature newborns (9 days old)were observed. Sleep propensity was defined as occur-rences of wakefulness; these were measured alongsidethermal recordings of abdominal and distal regions (foot,thigh and hand). The differences between the temperaturemeasurements were defined as peripheral vasodilation. Re-sults showed that shorter durations of sleep propensitycorrelated with higher temperatures of distal areas and thechest, associated with moderate vasodilation within theareas mentioned. The authors concluded that distal skintemperatures influence sleep onset in premature infants.Kurath-Koller et al. [37] studied thermal changes that

occurred during laser acupuncture to evaluate the safetyof laser acupuncture in neonates. Overall, 20 infants,with a mean age of 35 gestational weeks, were studied.Before laser acupuncture was performed, thermogramswere taken of both hands. Vital signs were also recorded.An increase in temperature was observed on both hands.The maximum temperature measured was 38.3 °C forthe right and 38.7 °C for the left hand. Vital signsshowed no significant change. As none of the neonateshad significant differences in thermal distributions, itwas concluded that acupuncture is safe to be used onneonates. Nonetheless, the authors note that warming ofskin during or after the procedure ought to be treatedwith care.

Technical concernsDespite the increasing use of TI applications in neonatalcare, thermography has several methodological chal-lenges. In a study conducted in 1997, the infants were

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placed in an incubator, in order to maintain thermal sta-bility during consecutive recordings. To overcome thebarriers created by the materials that could intervene be-tween the camera and the infant, researchers made a10x15cm window in the canopy. To avoid any heat lossand influences of ambient temperature, the window wassealed with a polyvinyl cloth that enclosed the camera[32]. In 2013, in a study where the maturation of bodytemperature control in preterm infants was investigatedwith different temperature instruments, some specificchallenges were reported, as they assessed infantshoused in plexiglass incubators [35]. The sheet of poly-urethane that was used to prevent heat loss resulted in ablurred image, and therefore had to be replaced with aplastic sheet that was secured with tape. In this study,valid and reliable measures were obtained, so the au-thors concluded that a well-structured methodology withan appropriate camera for this specific environmentcould provide beneficial research opportunities relatedto body temperature and peripheral perfusion from birthin extremely low birth weight infants [35]. Other reporteddifficulties included water droplets on the polyurethanesheet, the type of camera, which was not cordless and hadto be connected to a laptop, the limited lens depth andthe small port-hole of the incubator [8, 35, 38]. Inaddition, although an ideal condition is a newborn that isperpendicular to the line-of-sight, achieving this is not al-ways possible. Optimising the viewing angle condition andthe selected field of vision, taking account of the wellbeingof the newborn and any clinical imperatives, is an import-ant consideration for correct measurements [41, 42].

DiscussionThis scoping review provides an overview of currentknowledge relating to the potential for TI applications inneonatal care. Our search was limited to the English lan-guage only, as no funds were available for translation.Excluding languages other than English may introduce alanguage bias and lead to erroneous conclusions, andsuch exclusions are not part of our usual practice whenundertaking systematic reviews. However, translation oftechnical data from basic science and technical studies islikely to be more complex than for other types of stud-ies, and there is no a priori reason to assume that tech-nical studies carried out in different languages wouldgenerate different results.All the studies but one that were eligible were case

series or observations on a series of infants. In the onlystudy that was described as a comparative cohort study,the age variable of the patients groups was not similar tocontrol group, which means that the participants assignedto the two groups were not representative of the samepopulation. Most of the studies had small cohorts or limi-tations of case reports’ intrinsic methodological problems,

while others presented heterogeneous samples. Despitethe generally promising nature of TI results since the earlyseventies, a large-scale study or a well-designed compara-tive cohort study appears to be missing from the currentliterature (Table 1). The range of health care facility con-ditions in the included studies means that is impossible toassume that the same recording environment was presentfor all the infants. Also, there were differences betweenthe age of the neonates, their underlying conditions, typesof incubators and radiant warmers [25, 34, 38].An infant exchanges heat with the environment via

the respiratory tract and the skin. Five of the includedstudies demonstrated that TI is a promising method forthe continuous monitoring of respiration and the en-ergy/heat loss, especially in intensive care units, openingthe road for further studies and adding new knowledgein the field of neonatal monitoring [17–19, 28, 34].However, as these studies had either a small sample size(max n ≤ 16 [28]), or the examination was conducted insub-groups [17], a further investigation in a bigger co-hort, with a standardised protocol and homogeneity inthe procedures and participants is needed.TI showed very good results in the investigation of

mother/infant skin-to-skin physiological effects, by pro-viding excellent results while being totally non-contact[17, 36]. As skin-to-skin has been proposed as an opti-mal approach for keeping premature babies heat stable[36], TI could be a method that will offer an in-depthunderstanding and facilitate further research in the field.Additionally, TI showed good results and future po-

tential as a method of continuous surveillance of neo-nates and their body temperatures for the identificationand monitoring of NEC, which is one of the most com-mon neonatal gastrointestinal emergencies, with a mor-tality rate of 15–30% [8, 25, 33, 38]. The imagingmethods currently used for this purpose (abdominalradiography and abdominal ultrasonography) have sev-eral limitations and do not always detect early or subtlesigns of NEC. The gold-standard abdominal radiographylacks sensitivity and specificity to the changes seen inNEC, especially in early stages [25]. Oh et al. [43] pub-lished an overview of several non-invasive technologiesthat has been used or tested for the detection of NEC(magnetic resonance imaging, gastric tonometry, pulseoximetry, near infra-red spectroscopy etc.), stating thatall of them have significant limitations and further adaptionis required. Herry et al. (2011) [25] proposed a method-ology that revealed very good results, by using abdominaltemperature to classify healthy infants and those with NEC,reporting a correct classification rate of > 90%. Other stud-ies suggested that the in-depth understanding of skintemperature and perfusion may provide a better insight intothe pathophysiology of NEC [8, 33, 38]. Additionally, theearly diagnosis and continuous observation of body

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temperature differences in neonates could significantly de-crease the length of hospitalisation and medical cost [8].Since the infant’s internal organs are poorly insulated,

almost forty years ago, Pomerance et al. [9] and Bhatiaet al. [31] reported that TI has the potential to identifypathologies in highly vascular deep-lying organs like theheart and the kidneys [9] and being used for follow-upexaminations in liver diseases [31]. Although the find-ings were promising, and it might be especially relevantfor premature newborns, whose body fat is lower, theseobservations were not pursued again by researchers untilthere was a sudden surge of interest/publications be-tween 2008 and 2011 [8, 26, 32, 37]. Nevertheless, nosimilar studies were identified since 1977. One reasonfor this could be that TI cameras used to be very expen-sive and the method has not generally been popular inthe medical field, as it was mainly used in industrial andmilitary applications [8, 26, 44]. A reduction in the costof the cameras, and an increase in quality has led to anupsurge of interest in TI in medical applications. Frombulky devices and gray scale low resolution images, thetechnology has moved to affordable and portable highspeed and resolution cameras, with thermal sensitivity(NETD-Noise Equivalent Temperature Difference) of <15mK in some cooled cameras. Additionally, radiometricimages provide the opportunity for sophisticated analyt-ics. As a result, and knowing that TI is a completelynon-invasive method there has been a very recent re-naissance of interest for using this method in medicalapplications [44]. It is worth mentioning that early cam-eras were not able to record temperature values, andtherefore researchers had to use a separate thermometer(usually a skin thermometer) to record temperaturevalues in combination with an infrared camera to makethermal images (recordings of infrared emission varia-tions). In addition, to display the images, researchers hadto use a polaroid photographs or similar photographsand usually the analysis was performed with a densitom-eter using a standard black body scale [27–30]. Recentdevelopments in TI equipment have overcome theseproblems, meaning that this area could now be veryready for research investment.Despite the described developments, TI applications in

neonatology can be more technically challenging that inother medical fields. The particular barrier is the use ofradiant warmer and incubators, as other heat sources ormaterials with high reflectivity can affect the recordings[14, 18, 45]. However, radiant warmers and incubatorsare essential, as they secure the maintenance of a ther-mally stable environment, which is a key task in neonat-ology [2–4, 8, 9, 18, 38, 41]. To accommodate theenvironmental confounders, the main methods for theassessment of a neonate’s body temperature when theyare in a controlled warmed environment include either

cable-bound sensors or sensors that require skin contact.The potential for mechanical stress has led cliniciansand researchers to investigate cable-free, non-contactand non-invasive methods [7, 10, 38, 42], and this is thecontext in which TI has been tested as a potential solu-tion. Two studies describe in detail the methodologybehind real-time TI assessment, highlighting the import-ance of the environment, settings and external sourcesfor accurate recordings [41, 42]. Both studies concludedthat a more reliable measurement protocol is needed.During the last years, infrared windows have been de-

veloped allowing the inspection or recording of closedareas. This can be a solution to the described difficultiesin comparison with the reported improvised windows[32, 35]. The infrared windows comprise Calcium Fluor-ide (CaF2) lenses (or other materials) that are able totransmit short, mid and longwave IR waves, and can beeasy installed on any surface [46, 47]. The infrared win-dows are the perfect solution for incubators, proving ahuge advantage and step change in development in TI ap-plications in neonatology, as they keep the environmentenclosed, and allow a TI camera to record continuously.

ConclusionA thermally stable environment and continuous bodytemperature recording are crucial factors in neonatology,for sick or preterm infants. This review demonstratesthat TI has potential for further development in thefield. Apart from the continuous measurement of theskin temperature and the ability to provide visual ther-mal maps from major body parts, TI appears to be ableto detect pathological conditions that include inflamma-tory responses. Despite, the almost 50 years of researchon the application of TI, and the generally positive re-sults obtained, research studies in big cohorts usingestablished methodological protocols are missing fromthe literature. The latest rapid development in thermalcameras, image analytics and other components offersgreat potential for future TI application in neonatology.

AbbreviationsFOV: Field of View; MBST: Mean body surface temperature; NEC: Necrotisingenterocolitis; NST: Non-shivering thermogenesis; SSC: Skin-to-skin care;TI: Thermal imaging; WHO: World Health Organisation

AcknowledgmentsThis article is based upon work from COST Action IS1405 BIRTH: “BuildingIntrapartum Research Through Health - An interdisciplinary whole systemapproach to understanding and contextualising physiological labour andbirth” (http://www.cost.eu/COST_Actions/isch/IS1405), supported by EU COST(European Cooperation in Science and Technology).The authors would like to acknowledge Professor Edward Bell (Professor ofPediatrics, University of Iowa) for his invaluable contribution to the currentstudy.

Authors’ contributionsAT conceived of the review, coordinated the review process and wrotethe first draft. NA conducted the search. AT, NA and SS independentlyselected the papers for inclusion (NA, SS: screening by title and abstract;

Topalidou et al. BMC Pregnancy and Childbirth (2019) 19:381 Page 12 of 14

AT and NA: full-text reviewing; AT and SS: references reviewing), extracted thedata and helped to draft the manuscript. SD made substantial contribution tothe design of the scoping review and to the final draft of the manuscript. Allauthors read and approved the final manuscript.

FundingThe authors did not receive any funding for this study.

Availability of data and materialsAll articles retrieved through standard university searches. All data used arepresented and included within the manuscript.

Ethics approval and consent to participateNot applicable

Consent for publicationNot applicable

Competing interestsThe authors declare that they have no competing interests.

Author details1Research in Childbirth and Health Unit, School of Community Health andMidwifery, Faculty of Health and Wellbeing, University of Central Lancashire,Preston, UK. 2Department of Neurology, Faculty of Medicine Novi Sad,University of Novi Sad, Novi Sad, Serbia.

Received: 25 September 2018 Accepted: 24 September 2019

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