A comparison of airway interventions and gastrostomy tube placement in infants with Robin sequence

Clinical

Paper

Craniofacial

Anomalies

A

comparison

of

airway

interventions

and

gastrostomy

tube

placement

in

infants

with

Robin

sequence

K.ElGhoul,C.E.Calabrese,M.J.Koudstaal,C.M.Resnick:Acomparisonofairway interventionsandgastrostomytubeplacementininfantswithRobinsequence. Int.J. OralMaxillofac.Surg.2019;xxx:xxx–xxx. ã2019InternationalAssociationofOral andMaxillofacialSurgeons.PublishedbyElsevierLtd.Allrightsreserved.

K.ElGhoul1,2,3_{,C.E.Calabrese}2_,

M.J.Koudstaal2,3,4_,C.M.Resnick3,4

1_{ErasmusUniversityMedicalCenter,}

Rotterdam,TheNetherlands;2Departmentof PlasticandOralSurgery,BostonChildren’s Hospital,Boston,MA,USA;3Departmentof OralandMaxillofacialSurgery,Erasmus MedicalCenter,Rotterdam,TheNetherlands;

4

HarvardSchoolofDentalMedicineand HarvardMedicalSchool,Boston,MA,USA

Abstract. Thepurposeofthisstudywastoevaluatefeedingimpairmentfollowing non-operativeoroperativemanagementofairwayobstructioninalargeseriesof infantswithRobinsequence(RS)byrateofG-tubeplacement.Aretrospective study was conducted at Boston Children’s Hospital including 225 patients (47.1%female)withRStreatedbetween 1976and2018.Subjectsweregrouped byinterventionrequiredforsuccessfulmanagementofairwayobstruction: non-operativeonly(n=120),tongue–lipadhesion(TLA,n=75),mandibulardistraction osteogenesis(MDO,n=21),ortracheostomy(n=9).Theoperativegrouphada higherrate ofG-tubeplacement(58.1%)thanthenon-operativegroup(28.3%, P<0.0001). Subjects in the TLAand tracheostomygroupshad higher oddsof G-tube placementthansubjectsintheMDOgroup:oddsratio(OR)5.5(95% confidenceinterval(CI)1.8–17.3,P=0.004)andOR27.0(95%CI3.2–293.4, P=0.007),respectively.Syndromicpatientsandthosewithgastrointestinal anomaliesalsohadhigheroddsofG-tubeplacement:OR3.5(95%CI1.7–7.2, P=0.001)andOR5.9(95%CI1.6–21.0,P=0.007),respectively.InfantswithRS whorequire anairwayoperationandthosewithasyndromicdiagnosisor gastrointestinalanomaliesaremorelikelytorequireplacementofaG-tube.Ofthe operativegroups,MDOwasassociatedwiththelowestG-tuberate,comparedto TLAandtracheostomy.

Key words:Robin sequence; airway obstruc-tion; mandibular distraction; tongue–lip adhe-sion; tracheostomy; feeding; failure-to-thrive; gastrostomy.

Acceptedforpublication

Robinsequence(RS),definedasatriadof

micrognathia, glossoptosis, and airway

obstruction, affects 1:3000 to 1:14,000

live-born infants1–7. Airway obstruction

andfeedingimpairmentaretypically

pres-ent at birth. Theairway obstruction can

oftenbemanagedwithproneorside

posi-tioning,supplementaloxygen,continuous

positive pressure ventilation, and/or

placement of a nasopharyngeal tube.

Some patients will require an operation

such as a tongue–lip adhesion (TLA),

Int.J.OralMaxillofac.Surg.2019;xxx:xxx–xxx

https://doi.org/10.1016/j.ijom.2019.10.013,availableonlineathttps://www.sciencedirect.com

mandibular distraction osteogenesis

(MDO), or tracheostomy. Airway

out-comes for MDO are superior to those

for TLA8,9. While tracheostomy is the

most effective procedure for relieving

airwayobstruction,theassociated

morbid-ityandcareburdentypicallyrelegatethis

operation to patients who are poor

candidates for or have failed alternative

operations10.

Infants with RS often have difficulty

with feeding and weight gain. Feeding

impairment may manifest as prolonged

feedingtimes,oxygendesaturationduring

feeding, dysphagia, gastroesophageal

reflux, and/or aspiration11,12. In some

patients,the highenergyexpenditure

re-quiredtoventilateinthefaceof

intermit-tent airway obstruction combined with

insufficient caloricintake duetofeeding

impairment will cause failure-to-thrive.

The mechanism of feeding impairment

in infantswithRS isunknown, butitis

hypothesized to be a direct effect of

breathing dysfunction.This is supported

byreportsofimprovementinoralfeeding

and weightgain following resolution of

airwayobstruction13–16.Mostinfantswith

RS willreceive caloric supplementation

vianasogastrictubefeedsforsomeperiod

duringearlyinfancy.Forthosewith

pro-longedoralfeedingimpairment,a

gastro-stomy tube (G-tube) is placed. G-tube

placement requires an operation and

exposesthepatienttoadditionalrisk17,18.

Theaimofthisstudywas toexamine

the rate of G-tube placement in infants

with RS, and to determine whether this

rate varies based on the type of airway

management. As airway obstruction is

theorizedtobethedirectcauseoffeeding

impairment in infants with RS, it was

hypothesizedthattherateofG-tube

place-ment would be higher in patients with

obstruction severe enough to require an

airwayoperationcomparedtothose

man-agednon-operatively.Furthermore,itwas

hypothesized that MDO, which relieves

airwayobstructionmorepredictablythan

TLA, would facilitate oral feeding and

therefore becorrelatedwithalowerrate

ofG-tubeplacement.

Materialsandmethods

Studydesignandsample

Thiswasaretrospectivestudyofpatients

whopresentedtoBostonChildren’s

Hos-pital (BCH)between 1976and2018for

the evaluation and management of RS.

Inclusioncriteriawere(1)adiagnosisof

RS (micrognathia, glossoptosis, and

air-way obstruction) by a member of the

Craniofacial Center, and (2) complete

recordsregardingairwayobstructionand

feedingduringthefirstyearoflife.

Exclu-sion criteria were (1) airway operation

after the first yearoflife,(2) more than

oneairwayoperation,(3)deathwithinthe

firstyearoflife,and(4)insertionofa

G-tube prior to an airway operation. All

subjects received non-operative airway

management such asproneorside

posi-tioning,supplementaloxygen,continuous

positive airway pressure(CPAP), and/or

insertion ofa nasopharyngealtube.

Sub-jectsweregroupedaccordingtothe

inter-vention(s)requiredduringthefirstyearof

lifeforsuccessfulmanagementofairway

obstruction: non-operative management

only (‘no operation’), TLA, MDO, or

tracheostomy. This study was approved

bytheInstitutional ReviewBoardofthe

Committee on Clinical Investigation at

BCH(Protocol#P00023123).

Decisions regarding airway

manage-ment were made by a multidisciplinary

careteamincollaborationwiththe

fami-lies. In patients with persistent airway

obstructionfollowingnon-operative

inter-ventionsanddemonstrationofairway

col-lapseprimarilyintheretroglossalareaby

endoscopic examination, either TLA or

MDOwasperformed.TLAwasusedprior

to 2014;from 2014 to2018, MDO was

used.Thischangewasbasedonareview

of TLA outcomes, which demonstrated

unpredictablereliefofairwayobstruction

withthisoperation9.Thedecisiontouse

TLAvs.MDOwasnotbasedonseverity

ofairwayobstructionorother

patient-spe-cificfactors.Inpatientswith

contraindica-tionstoTLAorMDO,multi-levelairway

collapse, and/or comorbidities requiring

long-termventilationandairway

suction-ing,tracheostomywasused.

Nasogastric tubes were inserted when

the diagnosisofRSwas madeand were

used eitherinlieuoforalfeedingorfor

supplemental caloricintake.Thefeeding

method,useofbreastmilkorformula,and

caloric intake goals were determined by

the neonatology andfeeding teams with

familyinput.Inpatientswithacleftpalate,

specialized feeding techniques were

taught by acleft-feeding nurse and

spe-cialtybottleswereprovided.Thedecision

toplaceaG-tubewasbasedonthe

expec-tationthatnon-oralfeeding

supplementa-tionwouldberequiredbeyond3months

duration.

Studyvariables

Theprimarypredictorvariablewastypeof

airway intervention.Secondary predictor

variables included demographic data,

presenceofcleftpalate,syndromic

diag-nosis,andneurological,cardiac,or

gastro-intestinal anomalies. The primary

outcomevariablewastherate ofG-tube

placement.

Statisticalanalysis

Descriptivestatisticswerecalculated.The

x

2

testandFisher’sexacttestwereusedto

comparetherateofG-tubeplacementand

categorical predictor variables between

groups. One-way analysis of variance

(ANOVA) was used to compare means

of continuous variables. Binary logistic

regression was applied to determine the

effectofpredictorvariablesonthe

prima-ry outcome variables, and odds ratios

(OR) with 95% confidence intervals

(95%CI) were calculated.AP-value of

<0.05wasconsideredsignificant.

Results

Atotalof341patientswithRSduringthe

studyperiodwereidentified.Ofthese,225

(47.1%female)metthecriteriafor

inclu-sioninthisstudy.Atotalof105(46.7%)

subjectshad an airwayoperation during

thefirst yearoflife:MDO,n=21;TLA,

n=75;tracheostomy,n=9.

A cleft palate was present in 214

(95.1%)subjectsandwasmoreprevalent

in the non-syndromic infants (98.4%)

than in the syndromic infants (91.2%,

P=0.013). There were no other

significant differences in predictor

vari-ablesbetweengroups(Table1).Atotalof

102(45.3%)patients had aclinical

syn-dromicdiagnosis,whichwasconfirmedby

genetic testingin 63 subjects(61.8% of

thosewithaclinicalsyndromicdiagnosis,

28.0%oftheentiresample).Stickler

syn-dromewas themostcommonsyndromic

diagnosis (n=33, 32.4%), followed by

22q11.2 deletion syndrome (n=6,

5.9%). Thirty-nine infants (38.2%) had

multipleanomalies notconsistent witha

known syndrome. Seventy-one infants

(31.6%) had extracraniofacial anomalies

including cardiac anomalies (n=47,

20.9%), neurological anomalies (n=33,

14.7%), and gastrointestinal anomalies

(n=21,9.3%)(Table2).

G-tubeplacement

A G-tube was placed in 95 subjects

(42.2%).Ofpatients whohadan airway

operation,61(58.1%)underwent G-tube

placement,comparedto34(28.3%)inthe

nooperation group(P<0.0001).Within

theoperativegroups,therates ofG-tube

placement were asfollows: MDO, n=7

(33.3%);TLA, n=46 (61.3%);

tracheos-tomy, n=8 (88.9%). Compared to the

MDO group, subjects in the TLA and

tracheostomy groups had significantly

higher odds for G-tube placement (OR

5.5, 95% CI 1.8–17.3, P= 0.004 for

MDO vs. TLA; OR 27.0, 95% CI 3.2–

293.4,P=0.007forMDOvs.

tracheosto-my)(Table3).

RatesofG-tubeplacementfor

second-ary predictor variables are shown in

Table 4. Patients with a syndromic

diagnosis had a higher rate of G-tube

placement than non-syndromic patients

for all groups (56.9% vs. 30.1%,

P<0.0001) (Fig. 1). Binary logistic

regression showed significantly higher

odds forG-tube placementinsyndromic

comparedtonon-syndromicpatients(OR

3.5, 95% CI 1.7–7.2, P=0.001). Those

with gastrointestinal anomalies also had

significantlyhigheroddsofG-tube

place-ment comparedtosubjectswithout such

anomalies (OR 5.9, 95% CI 1.6–21.0,

P=0.007)(Table3).

Discussion

Theresultsofthisstudyaffirmedbothof

the proposed hypotheses: the rate of

G-tubeplacementwassignificantlyhigher

in the operative groups than in the no

operation group (58.1% vs. 28.3%, P

<0.0001), and infants who had MDO

required a G-tube less frequently than

those who had a TLA (33.3% vs.

61.3%, P=0.023). Interestingly, infants

whohadatracheostomy,whichisthemost

effective operation to relieve airway

obstruction,hadthehighestrateofG-tube

placement. Thiscouldbe due to

institu-tional preference to place G-tubes in

patients with a tracheostomy or may

indicatethatthesubjectsinthe

tracheos-tomygroup hadamore severe

presenta-tion of airway obstruction and feeding

impairment than the other groups. The

latter is supported by the prevalence of

additionalanomaliesinthetracheostomy

group,whichweremore commoninthis

group thanintheother groups,although

statistical significance on this difference

wasnotreached(P=0.061).Neurological

anomalies were most common in this

groupandmayhavebeenassociatedwith

impaired swallowing function. Another

explanationmightbethatthefeeding

im-pairmentisprimarilyduetotheimpactof

glossoptosis on pharyngeal swallowing,

which is improved by TLA and MDO

butnotbytracheostomy.

Thepresentstudyfindingssupport the

hypothesis that feeding impairment in

infants with RS is a direct consequence

of breathing dysfunction. Adequately

addressingrespiratorysymptomsinthese

infants can lead to an improvement in

nutritional andcaloricintake. Inparallel

tootherreportsoffeedingparameters,this

studyofG-tuberatesisparticularly

infor-mativegiventhemoreinvasivenatureof

gastrostomiescomparedtoothermeansof

supplementalfeedingandthe

comprehen-sive comparisonofinterventions17,18. Of

the operative interventions, MDO was

associated with the lowest G-tube rate.

Inadditiontoimprovedfeeding

parame-ters,itssuperiorityoverTLAanduseasa

meanstoavoidtracheostomyinthemost

severely affected infants indicate that

MDO may represent the treatment of

choice inthosewithanoperative

indica-tion.TheG-tuberatesassociatedwitheach

Table2. Frequencyofsyndromicdiagnosis.

Syndromicdiagnosis Number Percentage

Nounifyingdiagnosisa _{39 38.2%}

Sticklersyndrome 33 32.4%

22q11.2deletionsyndrome 6 5.9%

Craniofacialmicrosomia 2 2.0%

Fetalalcoholsyndrome 2 2.0%

Mobiussyndrome 2 2.0%

TreacherCollinssyndrome 1 1.0%

Nagersyndrome 1 1.0%

CorneliadeLangesyndrome 1 1.0%

Emanuelsyndrome 1 1.0%

VanderWoudesyndrome 1 1.0%

Other 13 12.7%

a

Presenceofmultipleanomaliesnotconsistentwithaknownsyndrome.

Table3. Binarylogisticregressionanalysisforsignificantpredictorvariablesandgastrostomy.

Variable OR 95%CI P-value Cardiacanomalies 1.6 0.7–3.5 0.233 Neurologicalanomalies 1.4 0.5–3.9 0.494 Gastrointestinalanomalies 5.9 1.6–21.0 0.007 Syndrome 3.5 1.7–7.2 0.001 TLAa 5.5 1.8–17.3 0.004 Tracheostomya _{27.0 3.2–293.4 0.007}

OR,oddsratio;CI,confidenceinterval;TLA,tongue–lipadhesion;MDO,mandibular distrac-tionosteogenesis.AP-valueof<0.05isconsideredsignificant.

a

TLAandtracheostomywerecomparedrelativetotheMDOgroup. Table1. Demographicvariablesandoperativedataforallgroups.

Variable Nooperation(n=120) MDO(n=21) TLA(n=75) Tracheostomy(n=9) P-value

Female 54(45%) 14(67%) 34(45%) 4(44%) 0.318 Cleftpalate 114(95%) 17(81%) 74(99%) 9(100%) 0.009 Additionalanomalies 38(32%) 5(24%) 23(31%) 5(56%) 0.390 Cardiacanomalies 23 5 16 3 0.683 Neurologicalanomalies 22 2 6 3 0.061 Gastrointestinalanomalies 13 2 5 1 0.721 Syndrome 58(48%) 12(57%) 28(37%) 4(44%) 0.301

Ageatairwayoperation(days),meanSD – 6461 2437 1610 0.001

Ageatgastrostomy(days),meanSD 81104 211131 4257 2015 <0.001

G-tubeplacement 34(28%) 7(33%) 46(61%) 8(89%) <0.001

Concurrent – 2 38 6 –

Postoperative – 5 8 2 –

respiratory treatmentmodalityreported in

thisstudyhighlighttheneedforconcurrent

considerationofbothrespiratoryandfeeding

parametersandservetoinformmanagement

strategiesforinfantswithRS.

The study results are consistent with

those ofother studiesreportedinthe

lit-erature. In a literature review including

370infantswithRSwhohadMDO,Zhang

et al.19 reported improved oral feeding

aftertheoperation,with87.0%ofpatients

achieving full oral intake at the latest

follow-up.Ofthe157patientstreatedwith

TLA, 70.0% achieved full oral intake.

Susarla et al.16 reported a lowerrate of

G-tubeplacementin30patientswhohad

MDO (16.7%) compared to 31 patients

after TLA (48.4%). The rates reported

in the present study are higher for both

MDOandTLA,highlightinginstitutional

differencesanddiscrepanciesinthecare

ofinfantswithRS.

Otherstudies also support the

conclu-sion that a syndromic diagnosis is

inde-pendentlyassociatedwithahigherG-tube

rate. Gary et al.20 _{reported improved}

weightgainafterMDOinnon-syndromic

patientsonly,withnopostoperative

feed-ingimprovementinsyndromicpatients.In

a systematicreviewoffeedingoutcomes

ininfantswhohadMDOformicrognathia,

Breiketal.21reportedfulloralfeedingin

93.7% ofthose with non-syndromic RS

comparedto72.9%ofthosewith

syndro-mic RS. In terms of G-tube rates, the

present study is novel in reporting this

associationforallinfantswithRS,

includ-ingthosewhocanbemanaged

non-oper-atively. This finding underlines the

importanceofanearlysyndromic

diagno-sis,asitaffectsthemanagementofairway

obstructionaswellasfeeding.

Of note, the study sample showed a

higher prevalence of cleft palate in the

non-syndromicgroupthaninthe

syndro-micgroup (98.4%vs.91.2%,P=0.013).

The presence of a cleft palate was not

associated with a higher G-tube rate

(42.5%vs.36.4%,P=0.687),likely

indi-catingadequatemanagementoffeedingin

the presence of a cleft palate for those

patientswhocantolerateoralfeeding.

Thisstudyhasseverallimitations.First,

due to the retrospective study design, a

causativerelationshipbetweenairway

ob-structionandfeedingimpairmentcouldnot

be determined. Also, the rate of G-tube

insertionwasused asa surrogatemarker

forfeedingseverity.Thedecisiontoinserta

G-tube, however, was based on several

factorsincludingfamilyandcareteam

pre-ferences;theassumptionthatinsertionofa

G-tubeindicatessevere feedingimpairment

maynotalwaysbeaccurate.Additionally,

surgicalinterventionwasusedinthisstudy

tosignifytheseverityofobstructiveapnea,

withtheassumptionthatpatientsmanaged

without an operation had less severe

obstruction compared to those who had

TLAorMDO,andthatpatientswhohad

a tracheostomy hadthe mostsevere

obstruc-tion.A prospectivestudyusingobjective

measurementsforfeeding(caloricintake,

weightgain)andairwayobstruction

(poly-somnography) will further improve our

understanding.Finally,BostonChildren’s

Hospitalisatertiaryreferralhospital,which

may have led to selection bias ofmore

complicatedpatients.

In conclusion, infants with RS who

required an airwayoperation, were

syn-dromic,and/orhadgastrointestinal

anom-alies were more likely to require

4 ElGhouletal.

Fig.1. Non-syndromicvs.syndromicRobinsequence.(Abbreviations:MDO,mandibulardistractionosteogenesis;TLA,tongue–lipadhesion.).

Table4. RatesofG-tubeplacementforsecondarypredictorvariables.

Variable Value Number PercentagewithG-tube P-value

Sex Male 50 42.0% 0.947 Female 45 42.5% Cleftpalate No 4 36.4% 0.687 Yes 91 42.5% Cardiacanomalies No 66 37.1% 0.002 Yes 29 61.7% Neurologicalanomalies No 73 38.0% 0.002 Yes 22 66.7% Gastrointestinalanomalies No 78 38.2% <0.0001 Yes 17 81.0% Syndrome No 37 30.1% <0.0001 Yes 58 56.9%

placementofaG-tubefor prolonged

en-teralfeedingcomparedtothoseinwhom

theairwayobstructionwasmanaged

non-operatively.Ofthoseinfantswhohadan

airway operation, MDO was associated

withthelowestrateofG-tubeplacement

andtracheostomywasassociatedwiththe

highest rate. The study findings

under-score the relationship between feeding

impairmentandairwayobstructioninRS.

Funding

The author(s)received no financial

sup-port for the research, authorship, and/or

publicationofthisarticle.

Competinginterests

The author(s) declare no potential

con-flicts of interest with respect to the

re-search, authorship, and/or publication of

thisarticle.

Ethicalapproval

This studywas approvedby the

Institu-tionalReviewBoardoftheCommitteeon

Clinical Investigation at Boston

Chil-dren’sHospital(Protocol#P00023123).

Patientconsent

Patientconsentwasnotrequired.

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Address: KhalidElGhoul DepartmentofOraland MaxillofacialSurgeryErasmus MedicalCenter DoctorMolewaterplein40 3015GDRotterdam TheNetherlands E-mail:k.elghoul@erasmusmc.nl