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www.jped.com.br

REVIEW

ARTICLE

Excessive

crying

in

infants

Ricardo

Halpern

,

Renato

Coelho

ChildDevelopmentOutpatientClinic,HospitaldaCrianc¸aSantoAntônio(HCSA),SantaCasadePortoAlegre,PortoAlegre,RS, Brazil

Received21December2015;accepted14January2016 Availableonline17March2016

KEYWORDS Excessivecrying; Infant;

Circadianrhythm; Infantilecolic

Abstract

Objective: Reviewtheliteratureonexcessivecryinginyounginfants,alsoknownasinfantile colic,anditseffectsonfamilydynamics,itspathophysiology,andnewtreatmentinterventions.

Datasource: TheliteraturereviewwascarriedoutintheMedline,PsycINFO,LILACS,SciELO, andCochraneLibrarydatabases,usingtheterms‘‘excessivecrying,’’and‘‘infantilecolic,’’as welltechnicalbooksandtechnicalreportsonchilddevelopment,selectingthemostrelevant articlesonthesubject,withemphasisonrecentliteraturepublishedinthelastfiveyears.

Summaryofthefindings: Excessivecryingisacommonsymptominthefirst3monthsoflife andleadstoapproximately20%ofpediatricconsultations.Differentprevalenceratesof exces-sive crying havebeen reported, ranging from14% to approximately30% ininfants up to3 months ofage. Thereis evidencelinking excessivecrying earlyinlife withadaptive prob-lemsinthepreschoolperiod,aswellaswithearlyweaning,maternalanxietyanddepression, attentiondeficithyperactivitydisorder,andotherbehavioralproblems.Several pathophysio-logicalmechanismscanexplainthesesymptoms,suchascircadianrhythmalterations,central nervous system immaturity, andalterationsin theintestinal microbiota. Severaltreatment alternatives havebeen described,includingbehavioral measures,manipulation techniques, useofmedication,andacupuncture,withcontroversialresultsandeffectiveness.

Conclusion: Excessivecrying intheearlymonths isaprevalentsymptom; thepediatrician’s attentionisnecessarytounderstandandadequatelymanagetheproblemandoffersupport toexhaustedparents.Theprescriptionofdrugsofquestionableactionandwithpotentialside effectsisnotarecommendedtreatment,exceptinextremesituations.Theeffectivenessof dietarytreatmentsanduseofprobioticsstillrequireconfirmation.Thereisincompleteevidence regardingalternativetreatmentssuchasmanipulationtechniques,acupuncture,anduseofthe herbalsupplementsandbehavioralinterventions.

© 2016 Sociedade Brasileira de Pediatria. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/ by-nc-nd/4.0/).

Pleasecitethisarticleas:HalpernR,CoelhoR.Excessivecryingininfants.JPediatr(RioJ).2016;92(3Suppl1):S40---5. ∗Correspondingauthor.

E-mail:ricardo.halpern@gmail.com(R.Halpern). http://dx.doi.org/10.1016/j.jped.2016.01.004

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PALAVRAS-CHAVE Choroexcessivo; Lactente; Ritmocircadiano; Cólicasdolactente

Choroexcessivodolactente

Resumo

Objetivo: Revisaraliteraturasobrechoroexcessivoembebêspequenos,cólicasinfantis,esuas repercussõesnafamíliaeafisiopatologiaeestratégiasdetratamentos.

Fontedosdados: Revisadasasprincipaisbasesdedados,Medline,PsycINFO,LILACSeSciELO eCochraneLibraryutilizando‘‘choroexcessivodolactente’’e‘‘cólicasdolactente’’.Foram selecionadasaspublicac¸õesmaisrelevantescomênfasenosúltimoscincoanos.

Síntesedosdados: Éumsintomacomumnosprimeirosmesesdevidaeémotivodecercade 20%dasconsultaspediátricas.Asprevalênciasdechoroexcessivovariamde14a30%nestes lactentes.Existemevidênciasligandoochoroexcessivonosprimeirosmesesdevidacom prob-lemasfuturosbemcomoaodesmameprecoce,ansiedade,depressãomaterna,TDAHeoutros problemascomportamentais.Distintosmecanismosfisiopatológicospodemexplicaressequadro clínico,comoalterac¸õesnoritmocircadiano,imaturidadedoSNC,ealterac¸õesnamicrobiota intestinal.Sãodescritosdiversasalternativasdetratamentodesdemedidascomportamentais, técnicasmanipulativas,usodemedicac¸ãoeacupunturacomresultadoseeficáciacontroversos.

Conclusão: Paraochoroexcessivonosprimeirosmesesénecessárioaatenc¸ãodopediatrapara oentendimento,manejodoproblemaeoferecersuporteparapaisemexaustão.Aprescric¸ão dedrogasdeefeitosduvidososepotenciaisefeitoscolateraisnãoéterapêuticapreconizada anãoseremsituac¸õesextremas.Aeficáciadostratamentosdietéticoseousodeprobióticos ainda necessitade confirmac¸ão. Existem evidencias incompletasa respeito de tratamentos alternativoscomotécnicasmanipulativas,acupunturaeusodesuplementoabasedeervase intervenc¸õescomportamentais.

© 2016 Sociedade Brasileira de Pediatria. Publicado por Elsevier Editora Ltda. Este é um artigo Open Access sob a licença de CC BY-NC-ND (http://creativecommons.org/licenses/ by-nc-nd/4.0/).

Introduction

Crying is a common symptom in the first 3 months of life and is responsible for approximately20% of pediatric consultations.Althoughinmostcasesthissymptomis self-limitedandof benignetiology,itisa sourceofstress and often leads parents and caregivers to exhaustion.1 Crying

is part of the normal development of a baby and

con-stitutes a form of communication with their caregivers,

althoughnonspecific,andcanbecausedbydifferentstimuli,

such as hunger, manifestation of discomfort or pain, or

simplythebaby’sneedtoapproachthecaregiverfor

emo-tional comfort and safety. Different prevalence rates of

excessive crying have been reported in several studies,

ranging from 14% to approximately 30% in infants up to

3 months of age.1,2 A meta-analysis performed with 22

longitudinalstudiesshowedevidencethatassociates

exces-sive crying and other regulatory difficulties (sleeping and

eating) in the first months of life with adaptive

prob-lems at school age, mainly related to attention deficit

hyperactivity disorder (ADHD) symptoms and associated

behaviors.3,4

In a cohort study in the city of Pelotas, infants

that had excessive crying in the first three months had

approximately 30% more behavioral problems than those

that did not have excessive crying, even after

con-trolling for all confounding factors.5 Additionally, it is

associated withearly weaning,and maternal anxiety and

depression.6---9

Definitions

and

classification

Inaclassicstudyaboutcryingininfants,Brazeltondefines excessivecryingasany amount ofcrying thatworries the parents,10 but the consensusdefinitionby severalauthors

arethe criteria defined by Wessel,11 known asthe ‘‘rule

of three’’ (crying spellsat least threehoursa day, three

timesaweekforthreeconsecutiveweeksandlastingthree

months).Evenwithaconsensus,thereisnosingledefinition

ofwhatshouldbeconsideredexcessivecrying.12Anattempt

atclassificationwascarriedoutusingthreecriteria: from

newbornupto4monthsofage, infantswithcrying spells

andirritabilityforthreeormorehoursaday, threedaysa

weekandatleastforoneweek,andnofailuretothrive,i.e.,

withoutanyconsequencesforthechild’sdevelopment.13An

examplewouldbeahealthy infant,agedupto3months,

whofeedswellandhasaprolonged,strident cryingspell,

whichcanlastuptoafewhours,writhingandbendingthe

kneesandthighsovertheabdomeneliminatinggases;the

childseemshungry,butdoesnotcalmdownafterbeingfed.

It is a crying spell without apparent cause and maybe a

manifestationofothermedicalconditions,self-limitedand

benign.

Although it has a benign etiology, it causes parental

stress,oftenleadingparentstoexhaustionwithoutsolving

theproblem,which,asa result,canleadparents totake

dangerousmeasuresinanattempttocalmtheinfant.14 In

additiontotheindiscriminateuse ofpainkillers and

(3)

excessivecrying withoutquick resolutionin infants isone

ofthecausesofshakenbabysyndrome.15,16

InstudybyBrazelton10 oftypicalinfants,excessive

cry-ingismeasuredinhours/day.Inthisstudy,themeancrying

timeofaninfantaged2weeksisonehourand45minutes,

andat 12weeksofage,themeantimeisuptotwohours

and45minutes;at 12weeks,themeantimedecreases to

onehour.Thesecryingspellsaremorefrequentinthelate

afternoon,withapeakoccurrenceat3---6weeksofage.

Over time, attentive caregivers begin to differentiate

whatmotivatestheinfant’scrying,buttheperceptionof

dis-comfortandsufferingoftenconfoundstheirinterpretation,

leadingtoanovervaluationandhinderingamorethorough

assessment. As a didactic characterization and

classifica-tion,thecryingcouldbedividedintothreecategories:(1)

normal/physiological; (2) excessive,secondary to

discom-fortor disease;and(3)without anapparentcause,where

colicisincluded.17

Colic

Colicisaclinicalmanifestation,forwhichseveralattempts at explanation have been made and of whose etiology stillremains unclear.18 The current understanding is that

infantilecolicisavariationofnormalityratherthana

patho-logical entity,12,18 and it is a phenomenon that stilllacks

furtherunderstanding,butitisanimportantmanifestation,

throughcrying,thataffects20---30%ofinfantsupto3months

of age.12 Aprospective study with ten yearsof follow-up

showed that excessive crying caused by colic may be an

earlymanifestationofsusceptibilitytorecurrentabdominal

pain,psychologicalproblems,andallergiesthatwillaffect

childhood.19

Amongthestudiesontheetiologyand

pathophysiologi-calmechanisms,thecurrentandmostacceptedhypothesis

isthatexcessivecryingiscausedduetoanimbalanceinthe

centralnervoussystemof theseinfants,supported bythe

factthatchildrenbornwithcentralnervoussystem

impair-menthave moreintensecrying spells,18 aswellasinfants

whose mothers or fathers have depression or those born

prematureor small for gestational age,20,21 who show an

increasedrisk of excessive crying during the firstmonths

of life. This hypothesis is based on the fact that these

groups,whonaturallyhavegreaterbiologicalrisk,arealso

at increased risk of developmental delays,which maybe

related to the immaturity of the central nervous system

(CNS)aswellasthedigestivesystem.

The circadian system plays an important role in the

CNS, and some studies associate this function with colic

andexcessivecrying.22 Thecircadiansystem,regulatedby

the hypothalamus, affects physiological activities such as

sleeptime,bodytemperature,feeding,andproductionof

hormonessuchasmelatonin;it maturesduring thefirst3

monthsoflife.Althoughnochangein totalhoursof sleep

hasbeendemonstrated,infantswithexcessivecryingshow

adifferentiatedpatterninrandomeyemovementsleepand

a fragmented sleep pattern.23 Additionally, cortisol does

notincreasesignificantlyonlyin casesofstress, asit also

shows a circadian rhythm, with an important role in the

process of waking in the morning;22 in a study with

con-trol group, including infants with and without colic, the

differencebetween them wastheabsence ofthe cortisol

circadianrhythminthegroupwithcolic.24

Theevidencethatsupportsthishypothesisisthatinfants

withexclusivebreastfeedinghavefewercolicspells;ithas

been observed that the nocturnal breast milk has higher

amountsof melatonin25 andthat theinfants tend tohave

longerandless-fragmentedsleep.Likewise,thereisa

vari-ationintheamountofmelatonininbreastmilk,whichmay

change according tothe mother’s mood26 and is possibly

relatedtostress.

Regarding nutritional intolerances, mainly the

intoler-ance to lactose or allergy to milk, and, indirectly, the

irritativesubstancestransmittedthroughbreastmilk,

sev-eralstudies suggest an insignificantparticipationof these

elementsinexcessivecryinginhealthyinfants,dividingthe

opinion of pediatric gastroenterologists.18 When an infant

haslactoseintoleranceorallergytocow’smilk,inaddition

tothecrying theinfantwillalsoshowotherclinical

mani-festations,andthusthecriteriaforcolicwillnolongerbe

valid, asthese infants are not healthy. Similarly, there is

no consensusin cases of gastroesophageal reflux and the

use of proton-pump inhibitors to reduce gastric juice, as

a procedure to relieve crying spells in infants with this

type of problem.27 In recent years, some studies focused

ontheassociationofintestinalmicrobiota,altered

intesti-nalmotility,andtheincreasedproductionofgases,causing

abdominalpainandresultingincrying.28---31Afterbirth,there

isagradualincreaseinthediversityoftheinfants’intestinal

flora, but in those withexcessive crying spells,

consider-ing the colic criteria, the diversity was lower and they

hadareducedamount ofbifidobacteriaandlactobacilli.28

Thecolonizationofgas-producingcoliformbacteriawas

sig-nificantly higher in children with colic spells in a study

of exclusively breastfed infants, with a predominance of

Escherichia coli.29 There is indication that there may be

an intestinal inflammatory reaction, in addition to lower

microbiotadiversityininfantswithcolicspells.31

Some newborns, while still in the nursery, can be

perceived as likely candidates to have excessive crying

spells,withincreased chancesof meeting thecriteriafor

colic.Theseinfantsaresensitive,withincreasedirritability,

prone to intense reactions and less adaptable, who take

longertocalmdownwiththeusualmeasuresofbeingheld

and cuddled.This situationcharacterizesthe influence of

the infant’s temperament, which is defined as a set of

characteristics relatedtothe typeof responsetostimuli,

their adaptive capacity(ability to calm down in stressful

situations),andactivitylevel.32,33Whenthisinfant,

charac-terizedby havingadifficult temper,finds anon-favorable

environment,withtenseandinsecurecaregivers whodeal

inadequately withtheinfant,the excessivecrying willbe

themostcommonmanifestationofdiscomfort.34,35 Studies

have been performed toverifywhether thedifficult

tem-per seenin adults,demonstratedbystructuralchanges in

their brains, may be predictive when observed in infants

withhyper-reactivetemperament.36

Even in infants without this a difficult temper, the

environmental factors that cause family disruption, such

as psychosocial problems and domestic violence, may be

relatedtoexcessivecrying.Theinfantactsasasignalerof

whatishappeningwiththeircaregivers,mainlythemother,

(4)

betterobservedinthecasesofpostnataldepression.20,37Ina

prospectivestudy,itwasshownthatstressduringpregnancy

was strongly related to excessive crying spells in infants

duringthefirst6monthsoflife.38

Diagnosis

Asinanyclinicalresearch,theassessmentbeginswitha his-toryofsymptomsdescribedbythefamily,providingdetails suchasfrequency,intensity,timeofoccurrence,and dura-tionofcrying.The complaintofexcessivecryingdemands fromthepediatrician a carefulassessmentof theinfant’s behaviorandreactions,andtheinteractionofparentsand caregivers. Italsodemands searching, wheneverpossible, for a triggering event or situationin the infant’s routine, evenifnotdirectlyconnectedtoit,suchasafamilystress situation(psychosocialfactorssuchasunemployment, mar-italcrises,mourning).Thewayparentsarriveanddescribe thecomplaint,associatedwiththedescriptionofhowthey holdandreceivetheirbabies,aswellasthestrategiesused tocalmthem,arean importantsourceofobservationand canbeusedtherapeuticallyduringtheconsultation.39 The

history and the motivation of the pregnancy and parents

facilitate the understanding,representation, andthe role

oftheinfantinthefamily.

During thephysical examination ofa small infantwith

excessivecryingthatmeetsthecriteriafor colic,itis not

common to find semiological alterations, but it is

indis-pensabletoperformacompleteexaminationaspartofthe

assessmentandasamanagementstrategy,inordertoensure

to parents that the infant does not have any associated

pathology. This procedure ensures the possibility of using

clinical reasoning tosearch, wheneverevident, for a

dif-ferentialdiagnosisamongthoselistedinTable1.Additional

testsarenotpartoftheresearchprotocolunlessthehistory

andphysicalexaminationsuggestssomepossiblecause.40

Clinicalmanagement

For clinical management, it is crucial to understand the complexity of symptoms and the possible causes, which in mostcases arenotexplicit. As inother behavioral and developmentmanifestations,theconceptofcumulativerisk effectcanbeappliedtoexcessiveinfantcrying.41 Mostof

the time, there is a set of factors with little individual

weight, but which together cause the clinical

manifesta-tion.Atfirst,itisnecessarytorecognizetheproblem,giving

supportandreassurance to thefamily, providing

informa-tionabout thebenign condition anditsnatural history,in

which95%ofcasesareself-limitedandonly5%haveprimary

causes.Informationaboutthenormalpatternofcryingand

theinfant’sself-regulatorymechanismshelptounderstand

the problem, as well as the necessary preventive

meas-ures against shaken baby syndrome and maltreatment.18

Often parents already show signs of fatigue and a few

areexhausted.Inextreme situations,theuseofnocturnal

emergencies services is frequent and, often, unnecessary

therapeuticmeasuresaretaken.

The necessary support to the family begins at the

consultationandwiththepediatrician’savailabilitytohelp

them.Thepediatricianmustbeattentiveandinterestedin

Table1 The mostcommon causesofexcessivecrying in younginfants.

Colic Noapparentcause,healthy infant,gainingweight,‘‘rule ofthrees’’

Infections Otitismedia;urinaryinfection; meningitis

Gastrointestinal Gastroesophagealreflux;reflux esophagitis;constipation; intestinalintussusception, lactoseintolerance,orallergy tocow’smilk

Trauma Cornealabrasion;foreignbody intheeye,‘‘toe-tourniquet’’ syndrome(strangulationof digits)

Behavioral/interactional Excessivestimulation,lackof routine,bondingdisorder Drugreactions Reactionstovaccines;drugs

usedduringpregnancy (narcotics)

Violence/abuse Longbonefractures;eye hemorrhage;intracranial hemorrhage

Hematological/ cardiovascular

Hemolyticcrisis--- sickle-cell anemia;tachyarrhythmia; congestiveheartfailure

Source:ModifiedandadaptedfromGrover.17

helping, and perform an adequate clinical assessment in

order to establish a secure baseline to confirm that the

infantishealthy.Thepositivereinforcementstrategyismost

effective when parents arehelped by the pediatrician to

findthesolutionstogether,ratherthanonlythetransferof

informationtothem.18

AccordingtotheWesselcriteriaforthediagnosis,theuse

oftheruleofthreesinthemanagementisalsouseful:(1)

infantilecolicisnotadisease;(2)nothingwillhappentothe

infantbecauseof thepain(dispelmyths);(3)colic passes

onitsownand‘‘itisaproblemthatthebabywilllearnto

solve’’(presentingthenaturalhistoryofthiskindof

prob-lem),relieving parentsfromtheresponsibility to‘‘solve’’

thecrying.42 Itisaneducationalprocessfortheparentsto

learntosolvecrises,clarifyingthemeaningsoftheinfant’s

crying,dispellingmyths,relievingfeelingsofguiltandthe

needtosharetheburden,whiletheotherrests.

It is essential to avoid the simplification of the

phe-nomenonandtheconsequentprescription ofcontroversial

drugs that have adverse effects, as well as exposing the

infanttounnecessarytestsandprocedures.Itisalso

impor-tanttodiscouragechangesintheinfant’sfeedingschemes,

suchasfrombreastmilktoinfantformula,aswellasfrom

theusual formula to differentbrands or sources,such as

soymilkorhydrolyzedformulas,withoutajustifiedclinical

basis.18Calmingthechildinoneoftheparent’sarms,orin

theproneposition,withawarmclothorusinghotwater

bot-tlestouchingthechild’sabdomenandabdominalmassage,

areproceduresthatshowsomeevidenceofcrying

improve-ment.Symptomimprovementwiththesetechniquesmaybe

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mother---infantbonding,sleeppatterns,andstresshormone

levels;43 nevertheless,placingtheinfantintheprone

posi-tioninthecribshouldbediscouraged,evenifthisposition

improves thecrying spells.18 The useof a pacifier canbe

occasionally allowed if it calms the infant; the relevant

guidelinesforusingthisresourcecanbeleftforlater.42

Some approaches have shown some evidence of

bene-fit,suchaswrappingthe infant,which hasbeenshown to

bemoreefficientthe youngerthe babyis, upto8weeks

ofage,whencomparedtothegroupthatwasnotwrapped.

Historicalreportsshowtheuseofthisprocedureinthepast;

themaineffectisincreasedsleepdurationanddecreased

motoractivity.44Similarly,theuseofsleephygieneandthe

establishmentofaroutine,organizingtheinfant’sandthe

parents’day, provedtobeeffective inreducingcrying by

42%.45Theuseofteas,suchasfennel,licorice,chamomile,

and peppermint, were part of a systematic review, and

some encouragingresults were shown using fennel versus

placebo46;sincetheydonothave sideeffects,theycould

beusedasatherapeuticaid.18

The prescriptionof drugsis controversial andtheiruse

shouldbediscouragedduetothelackofevidenceof

ben-efits,butinrarecases,suchasinafamilycrisis,withvery

highanxietylevels,sleepdeprivation,withoutafamily

sup-portnetwork, and withtheinfant at risk ofsuffering the

consequencesof familydysfunction, drugs canbe

tempo-rarilyused.Themostoftenrecommendedarephenobarbital

at a dose of 10mg three times/day or diphenhydramine,

6mg,twotothreetimes/day,bothfor oneweek, sothat

the initial approach steps can be resumed.12 The use of

simethiconeisnowwell-acceptedinclinicalpractice,more

frequently through self-medication, but it shows no

evi-denceofbenefit,47 and itseffectcouldbea consequence

ofthecalmingeffectofitssweettaste.46

It is noteworthy that the isolated use of drugs greatly

reducestheeffectof amorecomprehensiveandsystemic

approachtosolvingtheproblem.12

The use of probiotics is part of several studies and is

increasing as a promise of improvement in colic

symp-toms,buttheevidenceofitseffectivenessandtheresults

arecontroversial.48 Inarecentmeta-analysistherewasan

improvement in crying and treatment effectiveness, but

onlyaftertwotothreeweeks andtogetherwiththe

nat-uralhistory ofcolicimprovement.49 Inanothersystematic

reviewandmeta-analysisstudy,theimprovementoccurred

onlyinthegroupofinfantsthatwasbreastfedandthestudy

concludedthat thereis littleevidencetorecommendthe

useofprobioticsinthetreatmentofinfantswithcolic.30

Somealternative therapieshavebeen proposedforthe

treatment of colic and excessive crying, including

chiro-practic and cranial manipulation. A systematic review in

theCochrane database,although showing insome studies

areductionincolicsymptomsandcryingusingthese

tech-niques,doesnotallowtheclinicaluseoftheoutcomesdue

topotentialbiasesinthestudies.50

Another proposed treatment is acupuncture, but its

resultsarealsocontroversial,andfurtherclinicaltrialsare

recommendedtoelucidatetheeffectsofthisformof

ther-apyforexcessivecryingandinfantilecolic.51

Crying as a prevalent symptom is usually a form of

communicationinyoungandhealthyinfants.The

pediatri-cian’scarefulassessment inseparatingsymptomsthatcan

have another meaning besides crying is essential for the

emotionalhealth oftheinfant.Itisincreasinglymore

evi-dentthatthefirstyears,whetherhealthyornot,willdefine

thechild’sdevelopmentandoftentheirbehaviorin

adult-hood.Therefore,buildingatherapeuticcooperationthrough

empathywillallowthepediatriciantobeanactiveobserver

and effectively elucidate the issues related to excessive

infantcrying.41,52

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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Table 1 The most common causes of excessive crying in young infants.

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