Estimation of date of death through wound healing of an extraction socket: A case report

Case

Report

Estimation

of

date

of

death

through

wound

healing

of

an

extraction

socket:

A

case

report

Joan

Viciano

a,

*

,

Ruggero

D

’Anastasio

a,b

,

Cristian

D

’Ovidio

b

,

Sara

Costantini

b

,

Aldo

Carnevale

b

,

Luigi

Capasso

a,b

a

UniversityMuseum,‘G.d’Annunzio’UniversityofChieti–Pescara,PiazzaTrentoeTrieste1,Chieti,Italy

b

DepartmentofMedicineandAgeingSciences,‘G.d’Annunzio’UniversityofChieti–Pescara,ViadeiVestini31,66100Chieti,Italy

ARTICLE INFO Articlehistory: Received1March2016

Receivedinrevisedform27February2017 Accepted20March2017

Availableonlinexxx Keywords: Alveolus Toothextraction

Healingofextractionwound Alveolarboneremodeling Dateofdeath

Forensicinvestigation

ABSTRACT

Surgicalextractionofteethduetodentalpathologiesisarelativelycommonprocedureinmodernman.

Thehealingofthewoundthatresultsoccursingradualandsequentialstages,suchthattheanalysisof

thisrepairprocesscanbeveryusefulinforensicinvestigationsonhumanremains.Thefollowingstudy

reportsonaparticularcasewheretheremodelingofatoothsocketallowedanestimationofthetimethat

hadelapsedfromthedayofthesurgicalextractionofthetoothtothetimeofdeath.Thecorpsewasthat

ofawomanof34years.Itwasinanadvancedstateofdecomposition,asitwaslargelyskeletonized.

Macroscopic,radiographic,andhistologicalexaminationsoftheoralcavityshowedtheinitialstagesof

alveolarboneremodelingofthefirstleftmandibularmolar,whichwascharacterizedby:(i)asmall

reductionintheverticalheightofthevestibularsurfacewithrespecttothetheoreticaloriginalposition

ofthetooth;(ii)resorptionoftheintra-alveolarseptumandlaminadura;and(iii)formationofnew

immaturebone,whichcoveredtheentireinnersurfaceofthesocket.Thisstudyestablishedthatthe

subjectdied13–42daysafterthetoothextraction.Knowingthedateofthedentalextractionprovidedby

thepoliceinvestigation,itwaspossibletoprovideanestimateofthedateofdeath.

©2017ElsevierB.V.Allrightsreserved.

1.Introduction

AccordingtoDalitz[1],surgicaltoothextraction asa conse-quence of dental disease is a relatively commonprocedure in modernman.Healingoftheresultingextractionsocketappearsto progressinanorderedandsequentialmanner.Thiscanbeofgreat valueinforensicinvestigationsofunidentifiedhumanremains,as itcanprovidesomedegreeofaccuracyfortheestimationofthe period of time that has elapsed between the antemortem extraction of a particular tooth and the time of death of that person.Iftheidentitycanbeestablishedforhumanremainsthat have a healing tooth-extraction wound or have bone changes relatedtotherecentremovalofteeth,andifthedentalhistoryof thesubjectisknown,thenthisinformationcanprovidepositive contributory evidence, or indeed negative evidence, toward identificationofthetimeofdeath[1,2].

The aim of this paper is to report on a case where the remodeling of a tooth socket of a young woman allowed the

estimationofthetimethathadelapsedfromthedayofthesurgical extractionofthetoothtothetimeofthedeathofthesubject. 2.Casehistory

2.1.Discoveryofthecorpseandautopsyfindings

OnAugust26,2014,acorpsewasfoundamongweedsneara pylonunderaviaductoftheA14motorwaynearthetownofVasto (Chieti province,Italy).The corpsewas in anadvanced stateof decomposition, asit was largelyskeletonized. Inparticular, the cranium, thoraxandupperlimbswerecompletelyskeletonized, whilethepelvisandlowerlimbsshowedmummifiedsofttissues (Fig.1).Thesewerecharacterizedbyaparchment-liketexture(i.e., ‘oldleather’)andwerestronglyattachedtotheskeleton.External andinternalexaminationofthecorpserevealednopathological findings. Toxicological examinations did not reveal any extra relevantdetailsconcerninguseofalcoholorpharmaceuticals,orof drugsofabuse.

A few days later, the corpse was identified through DNA analysis. According to theinformation from thepolice and the forensicinvestigation,thecorpsebelongedtoawomanof34years whohadgonemissinginVastoonMarch28,2014.

* Correspondingauthor.

E-mailaddresses:joanviba@ugr.es,joanviciano@gmail.com(J.Viciano).

http://dx.doi.org/10.1016/j.forsciint.2017.03.008

0379-0738/©2017ElsevierB.V.Allrightsreserved.

ForensicScienceInternationalxxx(2016)xxx–xxx

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FSI8795No.ofPages6

ContentslistsavailableatScienceDirect

Forensic

Science

International

OnSeptember12,2014,atthemorgueoftheVastocemetery, ourexpertworkinggroupinphysicalanthropologyanalyzedthe corpsetoevaluatethepresenceofpossibleskeletalinjuriesand/or otherevidencethatmightbelinkedtothecauseofdeath.Thedelay betweentheautopsyandthephysicalanthropological investiga-tionwastheconsequenceoftheabsenceofinvolvementinChieti provinceof physicalanthropologistsin theinitial stages ofthe forensic work, including the recovery of skeletal remains, determinationofthepostmorteminterval,andtheidentification procedure.Whentheforensicinvestigationisatastandstill,the forensicpathologistwillsometimescontacttheforensic anthro-pologist.

2.2.Physicalanthropologicalexamination

Detailedmacroscopicexaminationofthemummi_fiedareasand thesingleboneelementsindicatedthattheywerewellpreserved, andthattherewerenosignsoftraumaticlesionsorotherskeletal evidencethatmighthavebeencorrelatedtothecauseofdeath. Duringthemacroscopicexaminationoftheoralcavity,theabsence ofninepermanentteethwasrecorded:threeinthemaxilla(i.e., secondleftpremolar,twothirdmolars),andsixinthemandible (i.e.,two first and second premolars, first left molar, third left molar)(Fig.2).Themacroscopicanalysisthatwascarriedoutin situinthemorgueofVastocemeterydidnotallowanyassessment ofwhethertheabsenceofthethreethirdmolarswasantemortem (i.e.,whethertherespectivesocketswerecompletelyremodeled) orwhethertheycorrespondedtoagenesia(i.e.,whethertheywere due tothelack of formation of the dental germs duringtooth development).Themaxillarysecondleftpremolarandthetwofirst and second premolars of the mandible were lost postmortem, becausetherewerenosignsofalveolarboneremodeling.However, it was notedthat thesocketof the mandibularleft firstmolar showedtheinitialstages of bone remodeling.This observation allowedthepossibilitytoascertainthetimeofdeathofthesubject if the dental history records of the missing person could be obtained.Therefore,ourinvestigationwasfocusedonananalysis ofthissinglesocket,whichisdetailedinthiscasereport.

After photographic documentation of the oral cavity, we proceededtoisolatetheregionthatcontainedthesocketofthe mandibularfirst molar using a vibrating saw, toallow a more detailedstudy in thelaboratory.The mandibularfragment was subjectedtomacroscopicmorphologicalexamination,and radio-graphic and histological analysis. A radiographic image of the anteroposterior view was obtained by X-ray analysis (45kV, 5 mAsH) at the Department of Radiology of the Villa Serena Hospital(CittàS.Angelo,Pescara,Italy),anditwasexaminedbya

radiologist. Histological sections of the untreated mandibular sample (non-decalcified and not embedded in resin) were produced using a microtome (SP1600; Leica) with a diamond blade.Therelevanttoothsocketwassectionedatthelevelofthe impressionofthemesialrootofthemolar.Unstainedthinsections of 60

m

m and 100

m

m thickness were obtained, which were observedat40magnificationunderanopticalmicroscope(BX41; Olympus). The images were captured using a digital camera (Moticam 2300) connected to the optical microscope. The histologicalsectionswereperformedbyphysicalanthropologists attheUniversityMuseumof‘G.d’Annunzio’UniversityofChieti– Pescara(Italy).

Fig.1.Detailofthethorax,cranium,andmandible.

Fig.2.(a)Maxillashowingtheabsenceofthreepermanentteeth:thesecondleft premolar,andthetwothirdmolars.(b)Mandibleshowingtheabsenceofsix permanentteeth:thetwofirstandsecondpremolars,thefirstleftmolar,andthe thirdleftmolar.Forboththemaxillaandmandible,thepremolarswerelost postmortem.Themacroscopicanalysis insitudidnot allowdeterminationof whether thethirdmolars were lostantemortem orthey wereagenetic. The mandibularleftfirstmolar(arrow)waslostantemortem,withinitialstagesofbone remodelingseen.

Thehealingphaseandtherelatedsurvivaltimeafterextraction wasestimatedusingthetimesequencesoftissueregenerationin humanextractionwoundsthathavebeenreportedintheliterature

[1–14].Complementaryanalyses(i.e.,degreeofdecompositionof thecorpse,forensicentomologyanalysis)werealsoperformedat theSectionofLegalMedicine(DepartmentofMedicineandAging Sciences,‘G.d’Annunzio’UniversityofChieti–Pescara),toestimate thedateofdeathofthesubject[15,16].

3.Results

3.1.Descriptionoftheobservedsignsofalveolarboneremodeling 3.1.1.Macroscopicdescription

Thealveolarridgewasatanearlystageofremodeling,andit showedaslightreductionintheverticalheightofthevestibular surfacewithrespecttothetheoreticaloriginalpositionofthetooth (Fig. 3a). Considerable remodeling activity was observed, with resorptionoftheintra-alveolarseptumandthelaminadura,and formation of new immature bone. This immature bone tissue coveredtheentireinnersurfaceofthesocket,whichincludedthe apical regions, the walls, and the region of the intra-alveolar septum(Fig.3b).

3.1.2.Radiologicaldescription

Thecorticalboneofthealveolarprocessshowedresorptionat thelevel ofthealveolarridgeandthewallsof thesocket.The intra-alveolar septumwas in the process of resorption, and a small degree of intra-alveolar radiopacity extended from the wallstothecenterof thesocket.Aboutaquarteroftheapical third of the socket was occupied by this radiodense tissue (Fig.4).

3.1.3.Histologicaldescription

Theentireinnersurfaceofthesocketwascoveredwithwoven bone, withsome osteocytesvisible within theimmature bone. Lamellar bone appeared to be absent. Most of the socket was emptyandhadprobablybeenoccupiedbyprovisionalconnective tissueandgranulationtissue,whichwouldhavedisappearedasa consequenceofthedecompositionprocess.

There werealso evident differencesin thecomposition and structuralorganizationofthereparativebonetissuecomparedto thebasalbonetissueofthemandible.Thebasalbonetissuewas fullyorganized,whilethenewlyformedtissuehadremainedvery unorganized(Fig.5).

3.2.Estimationofthetimeofdeathofthesubject 3.2.1.Woundhealingoftheextractionsocket

Weconsideredthedateofthetoothextractionprovidedbythe policeinvestigationasthereferencetime.Wewereinformedthat

thesubjecthadundergonedentalsurgeryonMarch15,2014,for extractionofthemandibularleft_firstmolar.

Accordingtotheradiologicalfindings,thetimethathadlapsed fromthetoothextractiontothedeathofthesubjectwasestimated to be between 21days and 38days [1_–4,6,13]. The histological analysissuggestsatimesequenceofosseousrepairoffrom13days to42days[4,5,7–14].Thus,themaximumrangeoftimebetween the toothextraction and thetime of deathof this subjectwas estimatedasfrom13daysto42days(Table1).Therefore,asthe toothextractiontookplaceinMarch2014,weestimatedthatthe deathofthesubjectwasmostlikelytohaveoccurredintheperiod betweenMarch28andApril26,2014.

3.2.2.Complementaryanalyses

Althoughthepoliceinvestigationheredidnotprovideanymore details, two independent and complementary analyses were

Fig.3.Mandibularfragmentcontainingthesocketoftheleftfirstmolar.(a)Vestibularsurfaceshowingasmallreductionintheheightwithrespecttothetheoreticaloriginal positionofthetooth.(b)Superiorviewofthesocketshowingextensiveboneremodelingactivity,withtheresorptionoftheintra-alveolarseptumandlaminadura,andthe formationofnewimmaturebonecoveringtheentireinnersurfaceofthesocket.

Fig.4. Radiologicalimageofthesocketoftheleftfirstmolar,showingresorptionof thecorticalboneofthealveolarprocessatthelevelofthealveolarridge,andthe wallsofthesocket.Theformationofnewimmatureboneisalsoseen,which occupiesaboutaquarteroftheapicalthirdofthesocket.

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performedtoestimatethedateofdeathofthesubject.Thesewere carriedoutbyresearcherswhowereblindedtotheresultsofthe previousanalysisduringtheirstudies,andtheywerebasedonan evaluationofthedegreeofdecompositionofthecorpse,andthe forensicentomologyanalysis.

Atthetimeofdiscovery,thedecayofthecorpsecorresponded tothefourthstage[15],when putriddestructionofthetissues occurs,andacorpseisgraduallyreducedtoaskeleton.Although theforensicliteraturedescribesmummificationasaprocessthat generallyoccursbetween6–12weeksfromthedeathofaperson, there are cases of premature mummification that have been describedincentralItaly,suchasthatofMarellaetal.[17],whose description matched the present case. The time of death was estimatedasatleast8weeksbeforethedateofthediscoveryofthe corpse,which establisheda temporalperiod of before June 31, 2014.

Fortheentomologicalevidence,severallivingspecimensand larvaeofColeoptera(i.e.,Corynetes,Staphylinidae)andLepidoptera werefound.Theirdetectionistypicalofthethirdsquadaccording tothe Mégnin classi_fication [16]. Based on this entomological evidence,the deathoccurred from3 to 6 months prior tothe

discoveryofthebody,whichdefinedtheperiodfromMarch28to theendofMay,2014.

Fig. 6 shows a summary of the chronological period of the eventsofthismedico-legalcase,andtheestimateddateofdeathof thesubjectaccordingtothedifferentmethodologiesused. 4.Discussion

Thesurgicalextractionofatoothinitiatesaseriesofreparative processesthatinvolvebothhardtissues(e.g.,alveolarbone)and softtissues(e.g.,periodontalligament,gingiva).Thesequenceof eventsthatleadtoalveolarhealingaftertoothextractionhasbeen extensively documented,asfollows[9,11]:(i)immediately after removalofthetooth,abloodclotwithatightfibrinnetworkfills the socket, and then polymorphonuclear cells and fibroblasts invade theclot; (ii) after2–3 days,granulation tissue starts to develop;(iii)onthefourthday,epithelialtissuegrowsoutfromthe edgesofthesocket,atwhichpointosteoclastsresorbthealveolar ridge;(iv)ontheseventhday,connectivetissuedevelopsatthe baseofthesocket,whichcontainsafewareasofosteoidtissue;(v) by day 20, re-epithelialization is complete, at which point mineralizationstarts,toproducewovenbone thatsubsequently undergoesremodeling;and(vi)40daysaftertoothextraction,the ridgeheightisdecreasedbyaboutonethird.

Althoughseveralstudies[e.g.,Refs.[1–14]]havedelineatedthe well-definedtendencyofeachtissuecomponenttochangeover time, theyhave alsorevealedcertain limitations, suchasgreat inter-individual variation with respect to tissue formation and maturation. In particular, it has been reported that whereas provisionalconnectivetissueappearstoformconsistentlywithin the first few weeks of healing, the interval during which the mineralizedboneislaiddownismuchlesspredictable[12].This variabilityinwoundhealingprocessesisalsoparalleledbyalarge variationinthedimensionalalterationstothehealingsocket.The reasonforthisvariationisatpresentnotunderstood,anditmight belinkedtodifferentfactors[14,18].Thesefactorsappeartobe,at least in part, related to: (i) the patient (e.g., smoking or local diseases,suchasadvancedperiodontaldisease,periapicalabscess, or granuloma [19,20]); (ii) the tooth site characteristics (e.g.,locationofedentuloussite,singleversusmultipleextractions

[21–23]),and(iii)surgicalvariables(e.g.,chlorhexidine adminis-tration following tooth extraction, elevation of a full-thickness

Fig.5.(a)Histologicalsectionatthelevelofthemesialrootofthesocket(magnification,40).Thedifferenceinthecompositionandstructuralorganizationoftherepair tissuecomparedtothebasalbonetissueofthemandibleisevident.Thebasalbonetissueisfullyorganized,whilethenewlyformedtissueisverydisorganized.(b)Thesame histologicalsectionunderpolarizedlight.

Table1

Estimation from the differentstudies of the time elapsed from thesurgical extractionofthetoothtothedeathofthesubject,accordingtothetimesequenceof osseousrepairofhumanextractionwounds.

Reference Timeelapsedfromdentalextraction(days) Kittner[3] <28 Mangos[4] 21–38 Swinburn[5] >14 Dawkins[6] >28 Amleretal.[7] 18–20 Dalitz[1] 21–28 Boyne[8] ca.13–16 Amler[9] ca.20 Evianetal.[10] 28–42 Bodicetal.[11] ca.20 Trombellietal.[12] 14–28 Marzolaetal.[13] 24–35 Morgan[2] ca.17–18 FarinaandTrombelli[14] ca.14–28 Maximumrangeestimated 13–42days

muco-periosteal flap) [24–26]. In the present case, there were signsofalveolarremodelingataninitialstage,thusminimizingthe inter-individualvariationofthetissueformationandmaturation thatisobservedinthelaterstagesofalveolarhealingthathasbeen describedinseveralstudies[e.g.,Refs.[12]].

Whilethestudiescitedabovecanyieldvaluableinformation, theyalsorevealcertainlimitationsfortheestimationofthetime sequence of tissue regeneration in the healing of extraction wounds,andtherefore,theymustbeconsideredwithcaution.The mainproblems concerningthemethodologicalaspects of these studiesrelateto:(i)inclusionoftissuesamplesfromsystematically diseasedindividuals,orevencadavers[e.g.,Ref.[4]];(ii)unclear,or non-standardized, experimental protocols [e.g., Ref. [7]]; (iii) evaluationofonlyafewtissuesamples[e.g.,Refs.[4,6,8]];and/or (iv)shortobservationintervals[e.g.,Refs.[7,8,10]].

However,notwithstandingtheselimitations,thetimesequence thathasbeendevelopedonthebasisofthesestudiesisuniversally acceptedbythescientificcommunity.Thisisusedasthebasisof discussionsofalveolarsockethealinginvariouscurrenttextbooks [e.g., Refs. [27–29]] and in the research literature [e.g., Refs.

[20,30,31]]. This time sequence thus forms the basis for the planning of definitive prosthetic, periodontal, and orthodontic clinicaltreatmentsthatfrequentlyfollowinseries,orarecarried outinconcurrencewithdentalextraction.

In this case report, the radiological methods indicated a narrower range of time between the tooth extraction and the deathofthesubjectthanthehistologicalmethods.However,there arenocomparativestudiesthatdemonstratethatsuchradiologyis statistically more precise or accurate than the histology. We applied both of thesemethods totake into account all of the possibilities,to providethe bestestimation of thepostmortem interval, and we consider the maximum range as the more appropriate.

5.Conclusions

Theoverall_findingsheredemonstratethatthehealingofthis surgical extraction socket followed a pattern similar to that describedintheliteratureaccordingtomacroscopic,radiological, and histological examinations of tissues harvested from socket sites in humans. Although the police investigation did not subsequentlyprovidetheexactdateofthedeathofthesubject,

thisstudyreportsacasewherealveolarboneremodelingallowed theestimationoftheperiodofdeath.Theestimatedpostmortem interval through wound healing of an extraction socket was consistentwith,andmorerestrictedthan,theevaluationfromthe degreeofdecompositionofthecorpseandtheforensic entomolo-gyanalysis.

Thus, tooth socket healing constitutes a potential source of informationfortheestimationofthetimethathaselapsedfrom thedayofsurgicalextractionofatoothtothetimeofdeathofthe subject,andthiswouldappeartobemoreprecisethanthedecayof thecorpseandtheforensicentomology.Withfurtherstandardized researchinthisdirection,theinformationthatcanbederivedfrom analysisofthewoundhealingofanextractionsocketcanprovidea valuabletoolforuseinmedico-legalcontexts.

Acknowledgments

The authors would like to thank Dr. Vincenzo Urbani and Department of Radiology of the Villa SerenaHospital (CittàS. Angelo, Pescara, Italy) for providing X-rays images of the mandibular fragment, and the UniversityMuseum of ‘G. d ’An-nunzio’UniversityofChieti–Pescaraforthetechnicalsupportand assistanceduringthehistologicalanalysis.

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