Classification of perinatal death...classification when gross necropsy findings were considered as well as clinical findings, and altogether only 21 (9%) changed classification when

Archives of Disease in Childhood, 1989, 64, 1345-1351

Classification of perinatal deathJ W KEELING,* I MAcGILLIVRAY,t J GOLDING,t J WIGGLESWORTH,l J BERRY,§ ANDP M DUNNt

*Department of Histopathology, John Radcliffe Maternity Hospital, Oxford, Departments of tObstetrics andtChild Health, University ofBristol, 1fDepartment ofHistopathology, Institute of Child Health, HammersmithHospital, London, and §Department of Pathology, Royal Hospital for Sick Children, Bristol

SUMMARY Three paediatric pathologists, one perinatal paediatrician, one obstetrician, and oneepidemiologist separately used information collected on 239 babies in an attempt to validate theWigglesworth classification of perinatal deaths. This was first done using clinical data only, thenusing the combination of clinical and gross necropsy findings and finally using clinical, grossnecropsy, histological and any other information (for example, chromosome analyses, micro-biological investigations). Only 14 (6%) of deaths changed groups within the Wigglesworthclassification when gross necropsy findings were considered as well as clinical findings, andaltogether only 21 (9%) changed classification when complete investigations were available.There was an unacceptable amount (15%) of disagreement between the classifiers, largely theresult of failure to comply with the rules laid down for classification. We set out amendments toWigglesworth's original definitions to clarify' certain ambiguities.

The number of classification systems of the causes ofperinatal death have increased over the years.Obstetricians' 2 have derived classifications thatdiffer substantially from those of pathologists.-7Paediatricians tend either to quote basic statistics,8or to use classifications derived by pathologistsrather than obstetricians.67 Despite the multiplicityof classifications, and firm but divergent opinionsabout which may be best, there has been littleassessment of the repeatability or the usefulness ofany of them.The aim of any classification must be to derive

strategies to understand the reasons for, and ulti-mately prevent, perinatal mortality. Wigglesworthargued that this was the only valid reason for aclassification.5 He suggested that any classificationshould be as simple as possible and presented insuch a way that the results give clear indications ofpriorities for prevention, and that the classificationshould be used to indicate the areas of health careprovision most in need of alteration. He put forwarda simple classification in which he allotted deaths toone of only five categories. It was devised so that itcould be applied with reservation to cases wherenecropsy investigation had not been undertaken,although he acknowledged that necropsy wouldpermit the most accurate categorisation.The simplicity of the classification is most attractive

and the fact that it can be used when necropsy hasnot been undertaken is helpful. Nevertheless,problems were encountered when it was used inone specialised unit9 and other problems wereencountered by one of us (JWK) in attempting toapply it to a regional study of perinatal mortalitywith a high necropsy rate.The present study was set up with three objectives:

firstly, to define more accurately the groups of theclassification, particularly in respect of problemsalready encountered; secondly, to investigate theextent to which classification of cases was changedby necropsy; and thirdly, to assess the reproducibilityof the classification when undertaken by people withan interest in perinatal medicine and pathology butwith different professional backgrounds.

Method

The six authors (three perinatal pathologists, oneperinatal paediatrician, one obstetrician, and oneepidemiologist) met first to discuss problems alreadyidentified in the Wigglesworth classification and todefine its groups more clearly. At a subsequentmeeting each member of the group was given theclinical, gross necropsy findings, and details offurther investigations of 233 perinatal deaths thathad been collected as part of a mtilticentre study of

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1346 Keeling, MacGillivray, Golding, Wigglesworth, Berry, and Dunn

perinatal deaths. Each member of the group wasasked to use the Wigglesworth classification andclassify the death firstly on the clinical informationalone, secondly on the clinical information togetherwith the findings from the macroscopic examinationat necropsy (which included the dissection of organs),and thirdly to classify the death taking account notonly of the clinical and necropsy findings but alsothe histological and microbiological examinations,and chromosome analyses.Each member of the team carried out the classi-

fication without knowledge of the classificationmade by the other members. After 89 perinataldeaths had been classified, the team met to discussproblems encountered and to compare results of theinitial classification exercise. At this stage there wassubstantial disagreement. For each case over whichthere was disagreement, extensive discussion tookplace to try and define more clearly the rules of theclassification. Once these rules had been delineatedmore clearly, the team was presented with a further144 cases to classify. Before this, the obstetrician(IM) had classified the 233 deaths using the Aberdeenclassification.2The following analyses of the data were carried

out: (i) identification of cases where there was stilldisagreement concerning the appropriate Wiggles-worth grouping; (ii) a study of all cases wherenecropsy and other results had made a difference tothe classification; (iii) a comparison of the classifica-tions made by all six observers of the last 144 cases(to give an estimate of interobserver reliability); and(iv) a comparison of the Aberdeen classificationwith the Wigglesworth classification, after takinginto account all necropsy and other findings.

Results

CLARIFICATION OF THE CLASSIFICATION

Group IThe original Wigglesworth group 1 was described as'normally formed macerated stillbirth'. After discus-sion the group was renamed 'deaths before the startof labour'. In the absence of other evidence, thepresence of maceration should be taken to indicatethat death preceded the onset of labour. Antepartumfetal deaths with lethal malformations were excluded,as were the miscellaneous disorders (see group 5).Much discussion concerned the distinction between

lethal and potentionally lethal malformations andminor malformations. It was suggested that macer-ated infants with minor isolated lesions (such as asmall ventricular septal defect) should remain in thisgroup, but that any infants with multiple minoranomalies (for example, cleft lip and a skeletal

defect) should be classified in group 2. Becausemany antepartum fetal deaths are associated withabruption, it was thought that a subgroup might beappropriate.

Group 2Group 2 was originally described as 'congenitalmalformations (stillbirth or neonatal death)'. Infantswith minor or potentially treatable minor malforma-tions should not be included here unless they formedpart of a complex of at least two malformations andthey had died before the start of labour. Deforma-tions-that is abnormalities of form secondary to afetal disease or functional impairment-could alsobe included here. Thus pulmonary hypoplasia thatfollows oligohydramnios may be included, althoughwe thought that this difficult diagnosis should alwaysbe supported by the presence of other deformationsor malformations.

Group 3Group 3 was described as 'conditions associatedwith immaturity (neonatal deaths only)'. It wasdecided that this group should be titled 'conditionsassociated with preterm birth or immaturity' andinclude only livebirths of under 37 weeks' gestation.

Infants weighing less than 1000 g should bepresumed to belong to this group irrespective of thetime of death. Larger preterm infants are likely tohave suffered from birth asphyxia if they die at lessthan 4 hours of age. Thus any infant dying at lessthan 4 hours, delivered preterm, and weighing morethan 1000 g, should be coded to group 4 belowunless a specific condition was present.

Neonatal deaths with infection, even congenitalinfection, should be included here if they weredelivered preterm, although specific infections-forexample, group B streptococcus and toxoplasma,other viruses, rubella, cytomegalovirus, and herpesvirus-should be coded group 5. The epidemiologist'sview was that if some infections remained in group 3,then all infections should stay in group 3. Thecounter argument was that 'important and interest-ing' infections should go to group 5.We came across problems with infants delivered

at full term but who had disorders normally asso-ciated with prematurity such as hyaline membranedisease, intraventricular haemorrhage, and necro-tising enterocolitis. It was decided that these shouldbe coded as group 5.

Group 4Group 4 in the original classification comprised'asphyxial conditions developing in labour (freshstillbirth/neonatal death)'. After discussion it wasdecided that this group should include all fetal

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deaths of whatever weight without malformationsor specific disorders, provided that fetal deathoccurred during labour. In the absence of otherinformation all fresh stillbirths should be included inthis group.

Liveborn infants weighing over 1000 g who died atless than 4 hours of age should be included in thisgroup. If the fetal death occurred during an inter-vention such as a caesarean section, in the absenceof labour, the case should be classed group 4, asshould any infants surviving longer than four hoursfor whom there was evidence of cerebral birthtrauma or asphyxia. Massive antepartum haemorr-hage such as abruption could form a clear sub-group.

Classification of perinatal death 1347

Group SGroup 5 was originally described as 'specific condi-tions other than above; and should include thefollowing: blood group incompatibilities, inbornerrors of metabolism, twin to twin transfusionsyndrome, hydrops not associated with malforma-tion, specific or unusual infections, conditions usuallyassociated with preterm delivery but occurring in ababy born at full term, tumours, hamartomas,neonatal deaths of term babies that are totallyunexplained, fetomaternal bleeds, or anythingcompletely out of the ordinary.

The decision tree evolving from the refinedclassification is shown in the figure.

Perinatal death

Lethal orpotentially I Yeslethalmalformation

4,No4,

Defined specificcondition Yes(see text)

No

Time of death

A1aAntepartum

IntrapartumN

Group 2

Group 5

X Group 4

Group 1

bLI

Neonatal

1000 g+

Died 4 hours+ -e

37+weeks' gestation

< 1000 g X- Group 3

Died <4 hours

Evidence of birthtrauma or asphyxia

<37 weeks' gestation

* Group 4

*+ Group 4

Group 3

Group 5

Figure Decision treefor the revised Wigglesworth classification.

+ 1)

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Table 1 Changes in Wigglesworth classification after necropsy and otherfindings had been reviewed

Case Classification CommentNo

Clinical Clinical Clinical,only plus necropsy plus necropsy,

plus otherfindings

10 3 4 4 Tentorial tear25 3 2 2 Congenital heart disease117 3 2 2 Congenital heart disease184 3 2 2 Congenital heart disease65 1 2 2 Congenital heart disease196 4 2 2 Congenital heart disease123 1 2 2 Gastrointestinal defect143 1 2 2 Congenital heart disease137 2 5 5 Clinical congenital heart disease; at necropsy idiopathic arterial

calcification155 2 5 5 Congenital heart disease-collapsed during catheterisation;

classified to iatrogenic181 1 5 5 Idiopathic arterial calcification151 4 4 5 Stormy labour, weighed 3580 g at 37 weeks, died at 7 hours.

PI haemolytic streptococcus grown204 4 5 5 Weighed 3640 g at 40 weeks; died at 2 days of pneumonia231 2 5 5 Antenatal scan showed cystic mass in neck; at necropsy non-rhesus

hydrops found175 4 5 4 At necropsy signs of sepsis found; on histological examination no sign

of sepsis97 3 3 5 ,B haemolytic streptococcus grown100 1 1 5 Congenital cocksackie A virus isolated145 1 1 5 Listeriosis290 3 3 2 Trisomy 21193 3 3 5 ,B haemolytic streptococcus grown244 3 3 5 Enzyme defect

CHANGES IN THE CLASSIFICATION AFTER NECROPSYOf the 239 cases considered, 14 (6%) were reclassi-fied once the gross necropsy findings were considered(table 1) and it can be seen that most were becauseof the discovery of congenital anomalies at necropsy.In addition, consideration of other data includingresults of histological and microbiological examina-tion further changed eight cases including one thathad changed between the clinical to the grossnecropsy classification (case 175). Interestingly, thiscase reverted to the classification that had beenbased on clinical grounds. Four of the other casesresulted from the identification of specific infections,one was an enzyme defect, and one a chromosomeanomaly. Thus in all, 21 (8%) cases were reclassifiedas a result of necropsy and other findings. It isunlikely that 8% of diagnoses would be changed ingeographic populations because the sample that westudied was not a representative series of perinataldeaths. It emanated from teaching hospitals withhigh rates of referral of complicated cases, and couldtherefore be expected to have a higher than normalproportion of unusual findings.

INTEROBSERVER RELIABILITYThe first sample of 89 cases were used as a learningexercise. The observers then compared results onthe subsequent 144 cases in order to assess repro-ducibility. In all, for each set of case notes, therewere 15 possible pairs of results. For each of thethree assessments (clinical only, clinical togetherwith gross necropsy, and clinical and all findings)there were 144x 15 x3-that is 6480 possible pairs..Disagreement at initial classification was found

for 963 pairs (15%). It should be noted that the 85%agreement rate is the interobserver variation anddoes not measure the accuracy of the classification.Major causes of disagreement concerned (i) whethera fetal death had actually occurred during labour,(ii) the class to which an immature infant should go,and (iii) how intrauterine infections should beclassified. Despite agreement beforehand aboutdefinitions, clinical experience tended to overridethem.

PROBLEM CASESOf the 233 cases considered there were 10 in which

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there was considerable discussion before eventualagreement. These are discussed below as examplesof the most difficult cases to classify.Case 16 was a diabetic cherub with visceromegaly

who died before the onset of labour. The problemwas whether this should be group 1 or 5; theultimate decision was group 5.Case 39 was a stillbirth that died before the onset

of labour. Clinically it was recognised as havingabnormal palmar creases and prominent heels,possibly as a result of a chromosome abnormality.At necropsy a solitary horseshoe kidney was found.The chromosome culture failed. This was eventuallyclassified as group 2.Case 51 was an infant born by caesarean section

for severe pre-eclampsia at 26 weeks. The babyweighed 510 g and died aged 1 day. There was

hydatiform change in the placenta. Should this begroup 3 or 5? As this is an unexpected and unusualfinding it was put into group 5.Case 53: liquor had been draining for weeks

since amniocentesis. The baby was born at 28 weeks'gestation, weighed 1160 g, and died at 90 minutes.Necropsy and histological examination confirmed a

congenital infection but no specific organism wasisolated. Various members of the team wanted toput it in group 3, 4, or 5. The rules, however, areclear and it was put into group 4.Case 72 was an infant delivered at 28 weeks'

gestation (1200 g) who died at 5 days. This was abreech extraction and the baby was clinically recog-nised as having aortic thrombosis with gangrene ofthe right toes and a flaccid left leg. Permission for afull necropsy was refused and external examinationonly was carried out. There was discussion aboutwhether this should be classified to group 3, 4, or 5,but it was finally put in group 5.

Classification of perinatal death 1349

Case 77 was a breech extraction at 27 weeksweighing 1271 g which died at 20 minutes. There hadbeen prolonged rupture of the membranes witholigohydramnios and the infant had hypoplasticlungs. The rules put this into group 4.Case 170 was born at 35 weeks' gestation weighing

1588 g. He had minor anomalies of the hands, limbs,and skull and died of massive pulmonary haemor-rhage and disseminated intravascular coagulation at7 days; this was put in group 3.

Case 186 was born at 37 weeks' gestation weighing2330 g, and died at 4 hours of age. At necropsy thebaby was found to have a polycystic right kidney,bilateral hydronephrosis and a double right ureter,and hypoplastic lungs. Gross necropsy examinationshowed a subarachnoid haemorrhage, hyalinemembrane disease, and pneumonia. Further investi-gations identified mycoplasma pneumonia. Thequestion was whether this should be classified asgroup 2, 3, 4, or 5. The team was divided, but therules indicated group 5.Case 212 was born at 36 weeks' gestation weighing

2240 g. It was dead at birth with mild hydrocephalusand undescended testes. Clinical notes stated clearlythat death was before labour. Labour was ofunknown duration. According to the rules thisshould have been coded as group 1 unless there wasdoubt as to whether the death occurred before orduring labour.Case 160 was born at 38 weeks' gestation weighing

2200 g and died at 4 days. There was cardiacmalposition, a single umbilical artery, undescendedtestes, and anomalous pulmonary segments. Thebaby died of a massive pulmonary haemorrhagewith a subarachnoid haemorrhage. There was muchdisagreement as to how this should be classified, butthe final decision was that it should be group 5.

Table 2 Aberdeen clinicopathological, and amended Wigglesworth, classifications after taking account ofclinical andnecropsy findings

Aberdeen classification Wigglesworth classification Total

1 (a) 1(b) 2 3 4(a) 4(b) 5

Premature, cause unknown 22 0 4 49 4 0 7 86Mature, cause unknown 11 0 1 0 9 0 1 22Mechanical 0 0 2 3 8 0 0 13Toxaemia. 4 0 1 10 2 0 1 18Antepartum haemorrhage 0 11 0 6 0 7 2 26Malformation 0 0 43 0 0 0 3 46Maternal disease 5 0 'O 1 0 0 1 7Rhesus incompatibility 0 0 0 0 0 0 6 6Miscellaneous 0 0 0 0 0 0 4 4Infection 0 0 0 1 0 0 4 5

Total 42 11 51 70 23 7 29 233

Subgroups (a) without and (b) with a history of abruption.

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RELATION TO OBSTETRIC CLASSIFICATION

The way in which the Wigglesworth classificationrelates to the Aberdeen classification is shown intable 2. It is clear that the two are measuringdifferent things. For example, of the 86 deathsclassified by the Aberdeen rules as 'premature cause

unknown' the Wigglesworth classification woulddistinguish the 22 dying before labour from the fourdying of intrapartum causes, and the 11 dying ofmalformations or specific disorders from the 49dying of disorders associated with immaturity.

Conversely, of the 30 that by the Wigglesworthclassification would have been coded as intrapartumasphyxia, the Aberdeen classification would havedistinguished the four 'premature-cause unknown'and the nine 'mature-cause unknown' from eight'trauma' and two 'toxaemia'.

Discussion

As different observers become more aware of theusefulness of classifying perinatal deaths to compareperformance over time and between centres, it is ofimportance to ensure that the classifications usedare repeatable. A recent publication showed thatthe Aberdeen obstetric classification, which hadbeen used for the Scottish National Survey and theNorthern Regional Health Authority Survey, alloweddifferences in its interpretation.10 These differenceshad developed both north and south of the borderduring the years since its introduction. The classi-fication has been in use for 30 years and only in 1986was a revised classification published with attentionpaid to current problems such as the death of thevery immature neonate.2 The authors concludedthat different assessors can classify a series of deathsin a similar way, provided that close attention is paidto the definitions and working rules. They foundthat different groups of clinicians reached similarconclusions in 97% of cases submitted for assessmentas long as they had a copy of the rules before them.

Nevertheless, there is considerable debate aboutthe interpretation of all classifications of perinataldeaths. As most classifications used in the UnitedKingdom are based either on the Aberdeen or

Wigglesworth classifications, we will confine our

discussion to these two. Table 2 shows that, ingeneral, the two classifications measure differentthings. Which is the more useful? Proponents of theAberdeen classification suggest that it is importantto know how many infants died from toxaemia, yetusing that classification one is unlikely to find thisout from the way the data are presented. Theclassification defines this group as having a diastolicpressure of 90 mm Hg or more on two separate daysafter 28 weeks' gestation together with appreciable

proteinuria, and in the absence of hypertensivedisease before pregnancy (which is comparativelycommon in pregnant women). Is it reasonable toassume that any normally formed baby born to awoman with this condition and dying prematurely isthe result of toxaemia? Prevention of pre-eclampsiain the mothers may not have prevented most of thesedeaths. Similarly, the Aberdeen classificationof 'trauma' (or under the revised classification,'mechanical causes'), covered deaths from birthtrauma and antepartum asphyxia associated withproblems in labour such as disproportion, mal-presentation, cord prolapse, cord compression, orbreech delivery in babies of 1000 g or more. If thereis no clinical history of difficulty in labour, butnecropsy evidence of trauma is present, the deathsare not classified as 'mechanical causes' but as'unexplained'. In other words, the trauma groupdoes not indicate the number of deaths with evidenceof birth trauma, but is a count of the number ofdeaths with abnormal presentation or method ofdelivery. It assumes that malpresentation is accom-panied by asphyxia and is thus responsible for death.Malpresentation is, however, common in smallbabies, so this group might just be an indication ofthe proportion of preterm infants.On the other hand, the Wigglesworth classifica-

tion does not, in its primary analysis, examinecauses of death in individual cases, so that sub-classification within the primary groups may benecessary. The classification relies heavily on gesta-tional age and time of death, and Wigglesworth hassuggested that a number of assumptions can bemade from these. A large number of deaths in group1 (antepartum stillbirths) suggests that more atten-tion to antenatal care might be warranted; manydeaths in group 2 (congenital malformations)perhaps indicates that more attention should begiven to preconceptional care; high numbers ingroup 3 (deaths associated with immaturity) mightsuggest that changes in neonatal intensive care werewarranted; a high proportion of deaths in group 4(intrapartum asphyxia) might indicate that obstetriccare could be improved. It is always anticipated thatgroup 5 will be a small group of miscellaneouscauses from which few generalisations could bemade, although it is a crude measure of the standardof perinatal histopathology, and other investigativeservices.

Since this study was carried out there has beenmuch discussion among the participants. Each stillprefers the classification that he has either developedor grown up with, but a majority were in favour ofthe revised Wigglesworth classification-perhapsbecause half the observers were perinatal patholo-gists. At the moment the topic of classification,

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Classification ofperinatal death 1351

especially the difference between the Aberdeen andthe Wigglesworth classifications, is largely a Britishphenomenon. Nevertheless, publications from manycountries are now appearing using the Wigglesworthclassification, interpreting the results to emphasiseareas in which medical care could be improved. 11-13

Classification should be precisely defined so thatit is easily applied by different people. In 10 cases(4%) no consensus was reached. This is too high,but most of these cases could have been classified bystrict adherence to the revised rules.Changes in classification occurred in 8% of cases

when information derived from the necropsy andthe results of all investigations were added to theclinical information. Though necropsy investigationscontribute to the accuracy of classification, theextent of change is modest and is certainly accept-able when the alternative is omission of deaths notcoming to necropsy. In most population studies thiswill be in excess of 30%.

Interobserver variability was 15%, and this degreeof disagreement is too high for most studies.Scrutiny of the results showed that many discrepan-cies resulted from one person failing to apply therules correctly, while 220 (23%) of the pairs ofdisagreement concerned the 10 cases that wereresolved after further discussion.We must reflect on the cause of the discrepancies.

Is the classification insufficiently precise for universalapplication, or were the classifiers at fault? It islikely that the answer is the second possibility.When classification is undertaken by those withprevious experience in a particular area it is likelythat they will be swayed by their experience ratherthan adhering to guide lines, however precise.Possibly the answer would be to have the codingdone by trained clerks rather than doctors, althoughthere are cases (as we have seen) in which consider-able judgment is required and it would be advisable

in these doubtful cases to have a consensus decisionfrom a medical panel.

References

Baird D, Walker J, Thomson AM. The causes and prevention ofstillbirths and first week deaths. Br J Obstet Gynaecol 1986;93:1204-12.

2 Whitfield CR, Smith NC, Cockburn F, Gibson AAM. Perinatallyrelated wastage-a proposed classification of primary obstetricfactors. Br J Obstet Gynaecol 1986;93:694-703.Claireaux AE. Perinatal mortality in the United Kingdom. In:Keller RJ, ed. Modern trends in obstetrics Ill. London:Butterworths, 1962:191-211.

4 Naeye RL. Causes of perinatal mortality in the US CollaborativePerinatal Project. JAMA 1977;238:228-9.Wigglesworth J. Monitoring perinatal mortality: a pathophysio-logical approach. Lancet 1980;ii:684-6.

6 Hey EN, Lloyd DJ, Wigglesworth JS. Classifying perinataldeaths: fetal and neonatal factors. Br J Obstet Gynaecol1986;93:1213-23.

7 Butler NR, Bonham DG. Perinatal mortality. First report of the1958 British Perinatal Mortality Survey. Edinburgh: ChurchillLivingstone, 1963.

8 Dunn PM, Vulliamy CB. Perinatal mortality statistics of theAvon County population (UK), 1976-1985 using FIGO 1982methodology. In: Kubli F, Patal N, Linderkamp 0, eds.Perinatal events and brain damage in surviving children. Berlin:Springer-Verlag, 1987.

9 Barson AJ, Tasker M, Lieberman BA, Hillier VF. Impact ofimproved perinatal care on the causes of death. Arch Dis Child1984;59:199-207.

10 Cole SK, Hey EN, Thomson AM. Classifying perinatal death:an obstetric approach. Br J Obstet Gynaecol 1986;93:1204-12.Tzoumaka-Bakoula C, Lekea V, McCarthy B, Golding J.Birthweight specific mortality in Greece. Acta Paediatr Scand1989 (in press).

12 Ashley D, McCaw-Binns A, Foster-Williams K. The perinatalmorbidity and mortality study of Jamaica. Paediatric andPerinatal Epidemiology 1988;2:138-47.

13 Sundhedsstyrelsen. Medicinsk fodsels-og misdannelsesstatistik1986. Vitalstatistik 1988;1:23.

Correspondence to Dr J Golding, Institute of Child Health, RoyalHospital for Sick Children, St Michael's Hill, Bristol BS2 8BJ.

Accepted 8 May 1989

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Classification of perinatal death...classification when gross necropsy findings were considered as well as clinical findings, and altogether only 21 (9%) changed classification when