Research
Stillbirth Facts
One of ANZSA’s key roles is to improve and
conduct research into stillbirth in the Australia and New Zealand region.
Research projects to date have been based around a range of areas such as
causes and risk factors, reduced fetal movement, unexplained stillbirth,
investigation, audit, classification, autopsy examination, and bereavement care
in a maternity hospital setting.
We have included a suite of general information outlining the key facts
surrounding stillbirth research for you. This information is the basis of a
more comprehensive report based on a systematic literature review which is
currently being undertaken by ANZSA with funding provided by the Stillbirth
Foundation Australia and the Department of Health and Ageing.
We hope this can enhance your knowledge, understanding and awareness of
stillbirth in Australia and New Zealand.
If you would like to find out more and/or would like clarification please
contact us at
info@stillbirthalliance.org.au The purpose of this overview is to provide general information to enhance
knowledge, understanding and awareness of stillbirth in Australia and New
Zealand on the causes, risk factors, investigation, audit and classification
and bereavement support for parents in the setting of maternity hospital care.
This overview forms the basis of a more comprehensive report based on a
systematic literature review which is currently being undertaken by ANZSA with
funding provided by
the
Stillbirth Foundation Australia and
the Department of Health
and Ageing. The final report from the review will conclude by summarising
the implications for practice and research toward the reduction of stillbirth
in Australia and New Zealand. In addition to this review, a number of studies
are currently underway which address current gaps in our understanding of
stillbirth.
For a summary of these studies please refer to the ANZSA stillbirth studies
registry.
We hope you find this overview helpful and we welcome
your feedback. This overview was initially prepared by: While infant mortality rates have declined in Australia over the past two
decades there has been no reduction in the rate of stillbirth. Stillbirths
account for 70% of perinatal deaths. Over 2,000 babies are stillborn in
Australia and New Zealand every year occurring at a rate of approximately 7 out
of every 1000 births; approximately 6 babies each day.
Stillbirth and
perinatal mortality statistics
For perinatal reports from across Australia and New Zealand please click here.
Globally, over 3 million babies are stillborn every year with the vast
majority occurring in developing countries (1). While less frequent in developed
countries (<1% of births), the large contribution of stillbirth to overall perinatal deaths
combined with static or increasing rates over the past decade (2), means
stillbirth remains a major public health problem in these settings.
Causes and risk factors for
stillbirth The reduction in the PMR seen in earlier periods was largely due to improved
intrapartum care resulting in less deaths from intrapartum asphyxia and birth
trauma, and also a reduction in deaths from isoimmunisation and diabetes (7, 8).
Congenital abnormality, unexplained fetal death and spontaneous preterm births
have now emerged as the leading causes of perinatal death in developed country
settings (9-12).
We are currently embarking on a large-scale prospective study across hospitals in Australia and New Zealand for raising DFM awareness using a mobile phone tool for pregnant women. See 'My Baby's Movements: a stepped wedge cluster randomised controlled trial of decreased fetal movement awareness to reduce stillbirth' on our Research Projects page. With decreasing perinatal mortality rates, the relative contribution of
antepartum fetal death where no cause for the death can be identified
[unexplained antepartum fetal deaths (UAFD)] appears to be on the increase (11).
The rates of UAFD reported internationally differ according to the definition
used however, it is estimated at 1-2 per 1000 births (41). The wide variation in
the reported contribution of unexplained stillbirth from 15% (42) to 71% (11)
has been attributed to the classification system (11, 43) and the thoroughness
of investigation and definition employed (41, 44). Lower rates of UAFD have
been attributed to more stringent diagnostic criteria used, specifically
autopsy and placental pathology examination (29).
Investigation,
audit and classification of stillbirth Determining the causes of stillbirth is an essential part of quality care
for parents and families. The purposes of investigations are to provide an
explanation for the death of their baby to the parents and family who need to
know what went wrong to relieve suffering, to enable appropriate counselling
about recurrence risk, and to inform the management of future pregnancies. An
accurate cause of death may assist in the parents grieving process by providing
an explanation for the death and other information on the circumstances
surrounding the death which may alleviate feelings of guilt (41, 46, 48, 52,
58). Even when a cause of death is not identified exclusion of some possible
causes is valuable as a reassurance to parents and to inform the planning and
management of future pregnancies (8).
Stillbirth
investigation protocols - current evidence PSANZ Stillbirth
investigation protocol Value of autopsy Autopsy quality
Information and
communication about perinatal autopsy All hospital perinatal autopsy examinations require written consent from the
parents following informed discussion(138). However, consent for autopsy is
difficult for both clinicians and parents. Parents face an apparently intrusive
process and are required to understand detailed consent procedures in a state
of grief and clinicians are reluctant to place further burden on the
parents (138, 146). Parents may think an autopsy will mutilate their baby (131),
that their baby has suffered enough or the parents may have religious
objections (130). In most cases, the medical consultant will approach the
parents for consent (131), however, midwives, nurses, social workers and
pathologists often have a role in providing information to assist in
decision-making (130, 131, 147).
Pilot data autopsy communication and information and planned study Support for parents
Stanton C, Lawn
J, Rahman H, Wilczynska-Ketende K, Hill K. Stillbirth rates: delivering
estimates in 190 countries. The Lancet. 2006 May, 2006;367:1489-94.
Smith GCS, Fretts RC. Stillbirth. Lancet. 2007;370:1715-25.
Li Z, Zeki R, Hilder L & Sullivan EA 2013. Australia's mothers and babies 2011. Perinatal statistics series no. 28. Cat. no. PER 59. Canberra: AIHW National Perinatal Epidemiology and Statistics Unit.
NZHIS. Report on Maternity: Maternal and Newborn Information 2002.
http://www.nzhis.govt.nz/publications/Fetal.html. Manatu Hauora:: Ministry
of Health, New Zealand Health Information Service (NZHIS); 2004.; 2004 Contract
No.: Document Number|.
AIHW NPSU 2003. Australian mothers and babies 2000. Canberra: AIHW
National Perinatal Statistics Unit (Perinatal Statistics Series no. 12); 2003
Contract No.: Document Number|.
Australian Institute of Health and Welfare. Australia's mothers and
babies 2000, Perinatal Statistics Series No 12. Sydney: Australian Institute of
Health and Welfare national perinatal statistics unit; 2003. Report No.: AIHW
Cat No PER 21 Contract No.: Document Number|.
Fretts RC, Boyd ME, Usher RH, Usher HA. The changing pattern of
fetal death, 1961-1988. Obstet Gynecol. 1992 Jan;79(1):35-9.
Goldenberg RL, Kirby R, Culhane JF. Stillbirth: a review.
J Matern Fetal
Neonatal Med. 2004 Aug;16(2):79-94.
Cernach MC, Patricio FR, Galera MF, Moron AF, Brunoni D. Evaluation
of a protocol for postmortem examination of stillbirths and neonatal deaths
with congenital anomalies. Pediatr Dev Pathol. 2004 Jul-Aug;7(4):335-41.
Flenady V, Chan A, Haslam R, King JF, Tudehope DI, McCowan L. Cause
specific perinatal mortality in Australia and New Zealand using a new clinical
classification system (ANZACPM and ANZNDC). Perinatal Society of Australia and
New Zealand 7th Annual Congress proceedings. Tasmania, Australia; 2003. p. A87.
CESDI - Confidential Enquiry into Stillbirths and Deaths in Infancy.
8th Annual Report. London: Maternal and Child Health Research Consortium; 2001
Contract No.: Document Number|.
Bell R, Glinianaia SV, Rankin J, Wright C, Pearce MS, Parker L.
Changing patterns of perinatal death, 1982-2000: a retrospective cohort study.
Arch Dis Child Fetal Neonatal Ed. 2004 Nov;89(6):F531-6.
Froen JF, Gardosi JO, Thurmann A, Francis A, Stray-Pedersen B.
Restricted fetal growth in sudden intrauterine unexplained death. Acta Obstet
Gynecol Scand. 2004 Sep;83(9):801-7.
Gardosi J, Kady SM, McGeown P, Francis A, Tonks A. Classification of
stillbirth by relevant condition at death (ReCoDe): population based cohort
study. Bmj. 2005 Oct 19.
Flenady V, King J, Gardener G, Charles A, Tudehope D, Coory M, et al.
Causes of fetal death in multiple pregnancies. Perinatal Society of Australia
and New Zealand Congress. 2006.
SOS-Forum. SIDS and kids: focussing on stillbirth. Investigation
and prevention of stillbirth. Setting the policy and research agenda. Sydney:
University of Sydney; 2001 November 29-30, 2001 Contract No.: Document Number|.
McDonald HM, Chambers HM. Intrauterine infection and spontaneous midgestation abortion: is the spectrum of microorganisms similar to that in
preterm labor? Infect Dis Obstet Gynecol. 2000;8(5-6):220-7.
Alfirevic Z, Roberts D, Martlew V. How strong is the association
between maternal thrombophilia and adverse pregnancy outcome? A systematic
review. Eur J Obstet Gynecol Reprod Biol. 2002 Feb 10;101(1):6-14.
Saade GR, McLintock C. Inherited thrombophilia and stillbirth. Semin
Perinatol. 2002 Feb;26(1):51-69.
McLintock LA, Jordanides NE, Allan EK, Copland M, Stewart K, Parker
A, et al. The use of a risk group stratification in the management of invasive
fungal infection: a prospective validation. Br J Haematol. 2004
Feb;124(3):403-4.
Rey E, Kahn SR, David M, Shrier I. Thrombophilic disorders and fetal
loss: a meta-analysis. Lancet. 2003 Mar 15;361(9361):901-8.
Dudding TE, Attia J. The association between adverse pregnancy
outcomes and maternal factor V Leiden genotype: a meta analysis; 2004 Contract
No.: Document Number|.
Perinatal Mortality Special Interest Group of the Perinatal
Society of Australia and New Zealand. Clinical Practice Guideline for perinatal
mortality audit. Brisbane, Australia: Perinatal Society of Australia and New
Zealand; 2004 Contract No.: Document Number|.
Fretts RC. Maternal age and fetal loss. Older women have increased
risk of unexplained fetal deaths. Bmj. 2001 Feb 17;322(7283):430.
Laws P, Sullivan EA. Australia's mothers and babies 2003. Sydney: AIHW National Perinatal Statistics Unit (Perinatal Statistics Series no. 16);
2005 Contract No.: Document Number|.
King Edward Memorial Hospital. Lessons from the enquiry into
obstetrics and gynaecological services at King Edward Memorial Hospital:
Australian Council for Safety and Quality in Healthcare; 2002 Contract No.:
Document Number|.
Heazell AE, Frxen J. Methods of fetal movement counting and the
detection of fetal compromise. Journal of Obstetrics and Gynaecology.
2008;28(2):147-54.
Froen JF. A kick from within--fetal movement counting and the
cancelled progress in antenatal care. J Perinat Med. 2004;32(1):13-24.
Froen JF, Arnestad M, Frey K, Vege A, Saugstad OD, Stray-Pedersen B.
Risk factors for sudden intrauterine unexplained death: epidemiologic
characteristics of singleton cases in Oslo, Norway, 1986-1995. Am J Obstet
Gynecol. 2001 Mar;184(4):694-702.
Fossen D, Silberg IE. [Perinatal deaths in the county of Ostfold
1989-97]. Tidsskr Nor Laegeforen. 1999;119(9):1272-5.
Maleckiene L, Nadisauskiene R, Bergstrom S. Socio-economic,
demographic and obstetric risk factors for late fetal death of unknown etiology
in Lithuania: a case--referent study. Acta Obstet Gynecol Scand. 2001
Apr;80(4):321-5.
Sadovsky E, Ohel G, Havazeleth H, Steinwell A, Penchas S. The
definition and the significance of decreased fetal movements. Acta Obstet
Gynecol Scand. 1983;62(5):409-13.
Olesen AG, Svare JA. Decreased fetal movements: background,
assessment, and clinical management. Acta Obstet Gynecol Scand. 2004
Sep;83(9):818-26.
Heazell AE, Sumathi GM, Bhatti NR. What investigation is appropriate
following maternal perception of reduced fetal movements? J Obstet Gynaecol.
2005 Oct;25(7):648-50.
Grant A, Elbourne D, Valentin L, Alexander S. Routine formal fetal
movement counting and risk of antepartum late death in normally formed
singletons. Lancet. 1989 Aug 12;2(8659):345-9.
Gribbin C, James, D. Assessing fetal health. Current Obstetrics and
Gynaeocology. 2005 01-105-2005;15:221-7.
Moore TR, Piacquadio K. A prospective evaluation of fetal movement
screening to reduce the incidence of antepartum fetal death. Am J Obstet
Gynecol. 1989 May;160(5 Pt 1):1075-80.
Heazell AE, Green M, Wright C, Flenady V, Froen JF. Midwives' and
obstetricians' knowledge and management of women presenting with decreased
fetal movements. Acta Obstet Gynecol Scand. 2008;87(3):331-9.
Heazell AE, Froen JF. Methods of fetal movement counting and the
detection of fetal compromise. J Obstet Gynaecol. 2008 Feb;28(2):147-54.
Flenady V, MacPhail J, Gardener G, Chadha Y, Mahomed K, Heazell AE,
et al. Detection and management of decreased fetal movements in Australia and
New Zealand: A survey of obstetric practice. Aust N Z J Obstet Gynaecol.
2008;Submitted.
Froen JF, Fretts RC, Gardosi J, Peterson K, Laurini R, Stray-Pedersen
B. IN-SI-DE, -International Interactive Inquiry on Sudden Intrauterine
Unexplained Death.
www.med.uio.no/inside; 2004 [updated 2004; cited 2004 24/02/04]; Available
from:
http://www.med.uio.no/inside/.
Gardosi J, Kady SM, McGeown P, Francis A, Tonks A. Classification of
stillbirth by relevant condition at death (ReCoDe): population based cohort
study. Bmj. 2005 Nov 12;331(7525):1113-7.
Korteweg FJ, Gordijn SJ, Timmer A, Holm JP, Rvaisi JM, Erwich JJHM. A
placental cause of intra-uterine fetal death depends on the perinatal mortality
classification system used. Placenta 2007;29:71-80.
Measey M, Charles A, d'Espaignet E, Harrison C, Douglass C.
Aietiology of stillbirth: unexplored is not unexplained. Aust NZ J Public
Health 2007;31:5.
Australian Bureau of Statistics 3303.0 (Online). Causes of death,
Australia, 2004. Available from:http://abs.gov.au/AUSSTATS/abs@.nsf/Lookup/3303.0Explanatory%20Notes12004?OpenDocument;
cited 2006 Contract No.: Document Number|.
Yudkin PL, Wood L, Redman CW. Risk of unexplained stillbirth at
different gestational ages. Lancet. 1987;1(8543):1192-4.
Flenady V, King J, Gardener G, Charles A, Tudehope D, Coory M, et
al., editors. Unexplained fetal death contribution: singleton vs multiples.
Perinatal Society of Australia and New Zealand Congress; 2006; Perth. Perinatal
mortality/Stillbirth investigation;.
Huang DY, Usher RH, Kramer MS, Yang H, Morin L, Fretts RC.
Determinants of unexplained antepartum fetal deaths. Obstet Gynecol. 2000
Feb;95(2):215-21.
Froen JF. Sudden intrauterine unexplained death. Oslo: Unipub AS;
2002.
Tolockiene E, Morsing E, Holst E, Herbst A,
Ljungh A, Svenningsen N, et al.
Intrauterine
infection may be a major cause of stillbirth in Sweden. Acta Obstet Gynecol
Scand. 2001 Jun;80(6):511-8.
Gardosi J, Francis A, R. S. Association between fetal growth
restriction and unexplained stillbirth at term. American Journal of Obstetrics
and Gynecology. 1999;180(1):S157.
Flenady V, Hockey RL, Chang A, Waters K. Unexplained fetal death at a
large maternity hospital: Identification of fetal risk factors: accepted for
publication. Perinatal Society of Australia and New Zealand 8th Annual
Congress.
Sydney; 2004.
Alessandri LM, Stanley FJ, Garner JB,
Newnham J, Walters BN.
A case-control study of
unexplained antepartum stillbirths. Br J Obstet Gynaecol. 1992 Sep;99(9):711-8.
Alessandri LM, Stanley FJ, Newnham J, Walters BN. The epidemiological
characteristics of unexplained antepartum stillbirths. Early Hum Dev. 1992
Sep;30(2):147-61.
Smith LL, Crowther CA, Lipsett J, Khong T. Unexplained Stillbirth-
Epidemiological, Social and Clinical Factors: A case controlled study.
Perinatal Society of Australia and New Zealand 6th Annual Congress proceedings.
Melbourne; 1999. p. A85.
Warland J, McCutcheon H, Baghurst P. Maternal Blood Pressure in
Pregnancy and Stillbirth: A Case-Control Study of Third-Trimester Stillbirth.
Am J Perinatol. 2008 Apr 28.
Smith GC, Pell JP, Dobbie R. Caesarean section and risk of
unexplained stillbirth in subsequent pregnancy. Lancet. 2003 Nov
29;362(9398):1779-84.
Dodd JM, Robinson JS, Crowther CA, Chan A. Stillbirth and neonatal
outcomes in South Australia, 1991-2000. Am J Obstet Gynecol. 2003
Dec;189(6):1731-6.
Diagnosis and management of fetal death. ACOG Technical Bulletin
Number 176-January 1993. Int J Gynaecol Obstet. 1993 Sep;42(3):291-9.
Pauli RM, Reiser CA. Wisconsin Stillbirth Service Program: II.
Analysis of diagnoses and diagnostic categories in the first 1,000 referrals.
Am J Med Genet. 1994 Apr 1;50(2):135-53.
Pauli RM, Reiser CA, Lebovitz RM, Kirkpatrick SJ. Wisconsin
Stillbirth Service Program: I. Establishment and assessment of a
community-based program for etiologic investigation of intrauterine deaths. Am
J Med Genet. 1994 Apr 1;50(2):116-34.
Royal College of Obstetricians and Gynaecologists and Royal College
of Pathologists. Fetal and perinatal pathology. London, UK: RCOG Bookshop; 2001
Contract No.: Document Number|.
Bove KE. Practice guidelines for autopsy pathology: the perinatal and
pediatric autopsy. Autopsy Committee of the College of American Pathologists.
Arch Pathol Lab Med. 1997 Apr;121(4):368-76.
American College of Obstetricians and Gynecologists. Genetic
evaluation of stillbirths and neonatal deaths. ACOG Committee Opinion.
2001;257:1-3.
Baird D, Wyper JFB. High stillbirth and neonatal mortalities. Lancet.
1941;2:657-9.
Baird D, Walker J, Thomson AM. The causes and prevention of
stillbirths and first week deaths. III. A classification of deaths by clinical
cause; the effect of age, parity and length of gestation on death rates by
cause. J Obstet Gynaecol Br Emp. 1954 Aug;61(4):433-48.
Pattinson RC, Makin JD, Shaw A, Delport SD. The value of
incorporating avoidable factors into perinatal audits. S Afr Med J. 1995
Mar;85(3):145-7.
Wigglesworth JS. Monitoring perinatal mortality. A pathophysiological
approach. Lancet. 1980 Sep 27;2(8196):684-6.
Chan A, King JF, Flenady V, Haslam RH, Tudehope DI. Classification of
perinatal deaths: development of the Australian and New Zealand
classifications. J Paediatr Child Health. 2004 Jul;40(7):340-7.
Whitfield CR, Smith NC, Cockburn F, Gibson AA. Perinatally related
wastage--a proposed classification of primary obstetric factors. Br J Obstet
Gynaecol. 1986 Jul;93(7):694-703.
Saasted E, Vangen S, Frxen F. Suboptimal care in stillbirths - a
retrospective study. Acta Obsetricia et Gynaecologica 2007;86(4):444-50.
De Lange TE, Budde MP, Heard AR, Tucker G, Kennare R, Dekker G.
Avoidable risk factors in perinatal deaths: A perinatal audit in South
Australia. ANZJOG. 2008;48:50-7.
Froen J, editor. Classification of stillbirth. International
Stillbirth Alliance Conference; 2006 June; Yokohama, Japan. Perinatal
mortality/Classification;Perinatal mortality/Stillbirth investigation;.
Korteweg FJ, Gordijn S, Timmer A, Erwich J, Bergman K, Bouman K, et
al. The Tulip classification of perinatal
mortality: introduction and multidisciplinary inter-rater agreement. BJOG.
2006;113:393-401.
Winbo IG, Serenius FH, Dahlquist GG, Kallen BA. NICE, a new cause of
death classification for stillbirths and neonatal deaths. Neonatal and
Intrauterine Death Classification according to Etiology. International Journal
of Epidemiology 1998 Jun;27(3):499-504.
de Galan-Roosen AE, Kuijpers JC, van der
Straaten PJ, Merkus JM.
Fundamental classification
of perinatal death. Validation of a new classification system of perinatal
death. Eur J Obstet Gynecol Reprod Biol. 2002 Jun 10;103(1):30-6.
Myers SA, Fisher DE, Moawad A, Paton JB, Lee KS, Ferguson M.
Assessment of potentially avoidable perinatal mortality in a regionalized
program. J Reprod Med. 1990 Jan;35(1):29-34.
Coria-Soto I, Zambrana-Castaneda M, Reyes-Zapata H, Salinas-Martinez
AM. Comparison of two methods for the discrimination of avoidable perinatal
deaths. J Perinat Med. 1997;25(2):205-12.
Richardus JH, Graafmans WC, Verloove-Vanhorick SP, Mackenbach JP.
Differences in perinatal mortality and suboptimal care between 10 European
regions: results of an international audit. Bjog. 2003 Feb;110(2):97-105.
Alberman E, Botting B, Blatchley N, Twidell A. A new hierarchical
classification of causes of infant deaths in England and Wales. Arch Dis Child.
1994 May;70(5):403-9.
Alessandri LM, Chambers HM, Blair EM, Read AW. Perinatal and
postneonatal mortality among Indigenous and non-Indigenous infants born in
Western Australia, 1980-1998. Med J Aust. 2001 Aug 20;175(4):185-9.
Hey EN, Lloyd DJ, Wigglesworth JS. Classifying perinatal death: fetal
and neonatal factors. Br J Obstet Gynaecol. 1986 Dec;93(12):1213-23.
H|ltin-Varli I, Hofsjv A, Bottinga R, Bremme K, Holm M, Holste C, et
al., editors. The Stockholm classification of fetal death. 2005 International
Stillbirth Conference; 2007; Washington, DC, USA.
Low JA, Boston RW, Crussi FG. Classification of perinatal mortality.
Canadian Medical Association Journal 1971 Nov 20;105(10):1044-6 passim.
Knutzen VK, Baillie P, Malan AF. Clinical classification of perinatal
deaths. S Afr Med J. 1975 Aug 16;49(35):1434-6.
Naeye RL. Causes of perinatal mortality in the US Collaborative
Perinatal Project. Jama. 1977 Jul 18;238(3):228-9.
Davies BR, Arroyo P. The importance of primary diagnosis in perinatal
death. Am J Obstet Gynecol. 1985 May 1;152(1):17-23.
Hovatta O, Lipasti A, Rapola J, Karjalainen O. Causes of stillbirth:
a clinicopathological study of 243 patients. Br J Obstet Gynaecol. 1983
Aug;90(8):691-6.
Borch-Christensen H, Langhoff-Roos J, Larsen S, Lindberg B,
Wennergren M. The Nordic/Baltic perinatal death classification. Acta Obstet
Gynecol Scand Suppl. 1997;164:40-2.
Fairweather DV, Russell JK, Anderson GS, Bird T, Millar DG, Pearcy
PA. Perinatal mortality in Newcastle upon Tyne1960-62. Lancet 1966;1
(7429):140-2.
Winbo IG, Serenius FH, Dahlquist GG, Kallen BA. A computer-based
method for cause of death classification in stillbirths and neonatal deaths.
International Journal of Epidemiology 1997 Dec;26(6):1298-306.
Chang A, Keeping JD, Morrison J, Esler EJ. Perinatal death: audit and
classification. Aust N Z J Obstet Gynaecol. 1979 Nov;19(4):207-11.
Stanley FJ, Hobbs MST. Perinatal outcome in Western Australia, 1968
to 1975. 3. Causes of stillbirths and neonatal deaths excluding congenital
malformations. Med J Aust. 1981;1:483-6.
Lammer EJ, Brown LE, Anderka MT, Guyer B. Classification and analysis
of fetal deaths in Massachusetts. Jama. 1989 Mar 24-31;261(12):1757-62.
Cole SK, Hey EN, Thomson AM. Classifying perinatal death: an
obstetric approach. Br J Obstet Gynaecol. 1986 Dec;93(12):1204-12.
Dickson N, Bhula P, Wilson PD. Use of classification of primary
obstetric factors in perinatally related mortality surveillance. N Z Med J.
1988 May 11;101(845):228-31.
Keeling JW, MacGillivray I, Golding J, Wigglesworth J, Berry J, Dunn
PM. Classification of perinatal death. Arch Dis Child. 1989 Oct;64(10 Spec
No):1345-51.
Alberman E, Blatchley N, Botting B, Schuman J, Dunn A. Medical causes
on stillbirth certificates in England and Wales: distribution and results of
hierarchical classifications tested by the Office for National Statistics. Br J
Obstet Gynaecol. 1997 Sep;104(9):1043-9.
Flenady V, King JF, Hockey RL, Tudehope DI, editors. The rationale
for clinical perinatal mortality classification - what more does it tell us
than ICD codes? Perinatal Society of Australia and New Zealand 3rd Annual
Congress Proceedings; 1999; Melbourne, Australia. Perinatal mortality;Unexplained fetal death;UXFD;.
Georgsdottir I, Geirsson RT, Johannsson JH, Biering G, Snaedal G.
Classification of perinatal and neonatal deaths in Iceland. A survey from a
defined population. Acta Obstet Gynecol Scand. 1989;68:101-8.
McIlwaine GM, Dunn FH, Howat RC, Smalls M, Wyllie MM, MacNaughton MC.
A routine system for monitoring perinatal deaths in Scotland. Br J Obstet
Gynaecol. 1985;92:9-13.
Morrison I, Olsen J. Weight-specific stillbirths and associated causes
of death: an analysis of 765 stillbirths. Am J Obstet Gynecol. 1985 Aug
15;152(8):975-80.
Baird D, Thomson A. The survey perinatal deaths re-classified by
special clinico-pathological assessment. In: Butler NR, Alberman E, editors.
Perinatal Problems The second report of the 1958 British Perinatal Mortality
survey. Edinburgh: Churchill Livingston; 1969. p. 200-10.
Butler NR, Bonham DG. Perinatal Mortality. The First Report of
the 1958 British Perinatal Mortality Survey. Edinburgh and London; 1963
Contract No.: Document Number|.
Maternal and Perinatal Infant Mortality Committee. Maternal and
Perinatal Infant Mortality in South Australia 2006. Adelaide: South Australian
Department of Health; 2007 Contract No.: Document Number|.
Kramer MS, Shiliang L, Zhongcheng L, Hongbo Y, Platt R, Joseph K.
Analysis of Perinatal Mortality and Its Components: Time for a Change? .
American Journal of Epidemiology 2002;156 (6):493-7.
PSANZ PMN-SIG. Perinatal Society of Australia and New Zealand: Special
Interest Group.
http://128.250.188.72/PSANZ/SIG/sig_intro.htm. Australia and New Zealand:
PSANZ; 2004 Contract No.: Document Number|.
King JF, Chan A, Haslam R, Tudehope DI, Flenady V, Hockey RL.
Classifications for perinatal death clinician agreement. Perinatal Society of
Australia and New Zealand 5th Annual Congress. Canberra, ACT, Australia; 2001.
p. 97.
Flenady V, Froen F, Pinar H, Torabi R, Saastad E, Guyon G, et al. An
evaluation of classification systems for stillbirth. BMC. 2008;Submitted.
Corabian P, Scott A. Protocols for stillbirth investigations.
Edmonton: Alberta Heritage Foundation for Medical Research; 2005 Contract No.:
Document Number|.
Agapitos E, Papadopoulou C, Kavantzas N, Papoulias J, Antonaki V,
Davaris P. The contribution of pathological examination of the placenta in the
investigation of the causes of foetal mortality. Arch Anat Cytol Pathol.
1996;44(1):5-11.
Cartlidge PH, Dawson AT, Stewart JH, Vujanic GM. Value and quality of
perinatal and infant postmortem examinations: cohort analysis of 400
consecutive deaths.
BMJ. 1995 Jan
21;310(6973):155-8.
Killeen OG, Burke C, Devaney D, Clarke TA.
The value of the perinatal
and neonatal autopsy. Ir Med J. 2004 Sep;97(8):241-4.
Kock KF, Vestergaard V, Hardt-Madsen M, Garne E. Declining autopsy
rates in stillbirths and infant deaths: results from Funen County, Denmark,
1986-96.
J Matern Fetal
Neonatal Med. 2003 Jun;13(6):403-7.
Rasmussen S, Albrechtsen S, Irgens LM,
Dalaker K, Maartmann-Moe H, Vlatkovic L, et al.
Unexplained
antepartum fetal death in Norway, 1985-97: diagnostic validation and some
epidemiologic aspects. Acta Obstet Gynecol Scand. 2003 Feb;82(2):109-15.
Rayburn W, Sander C, Barr M, Jr., Rygiel R. The stillborn fetus:
placental histologic examination in determining a cause. Obstet Gynecol. 1985
May;65(5):637-41.
Saller DN, Jr., Lesser KB, Harrel U, Rogers BB, Oyer CE. The clinical
utility of the perinatal autopsy. JAMA. 1995 Feb 22;273(8):663-5.
Cartlidge PH. Effect of changing the stillbirth definition on
evaluation of perinatal mortality rates. Lancet. 1995;346(August 19 -
8973):486-8.
Incerpi MH, Banks EH, Goodwein SN, Samadi R, Goodwin TM. Significance
of antinuclear antibody testing in unexplained second and third trimester fetal
deaths.
J Matern Fetal
Med. 1998;7(2):61-4.
Michalski ST, Porter J, Pauli RM.
Costs and consequences of
comprehensive stillbirth assessment. Am J Obstet Gynecol. 2002
May;186(5):1027-34.
Ahlenius I, Floberg J, Thomassen P. Sixty-six cases of intrauterine
fetal death. A prospective study with an extensive test protocol. Acta Obstet
Gynecol Scand. 1995;74(2):109-17.
Bohra U, Regan C, O'Connell MP, Geary MP, Kelehan P, Keane DP. The
role of investigations for term stillbirths. J Obstet Gynaecol. 2004
Feb;24(2):133-4.
Lim TLW TK, Tee SC, Yeo GSH. Investigating stillbirths using a
simplified obsettric events-based protocol. Arch Pathol Lab Med. 2005;130:62-8.
Incerpi MH, Miller DA, Samadi R, Settlage RH, Goodwin TM. Stillbirth
evaluation: what tests are needed? Am J Obstet Gynecol. 1998;178(6):1121-5.
Laube DW, Schauberger CW. Fetomaternal bleeding as a cause for
"unexplained" fetal death. Obstet Gynecol. 1982;60(5):649-51.
Flenady V, Gilshenan K, King J, Charles A, Coory M, d'Espaignet ET.
Investigation of Stillbirths. Conference Proceedings Perinatal Society of
Australia and New Zealand. 2008;April.
Khong TY. Ethical considerations of the perinatal necropsy. J Med
Ethics. 1996 Apr;22(2):111-4.
Gordijn SJ, Erwich JJ, Khong TY. Value of the perinatal autopsy:
critique. Pediatr Dev Pathol. 2002 Sep-Oct;5(5):480-8.
Khong T, Arbuckle S. Perinatal pathology in Australia after Alder Hey.
J Paediatr Child Health. 2002;38(4):409-11.
Rankin J, Wright C, Lind T. Cross sectional survey of parents'
experience and views of the postmortem examination. BMJ. 2002 Apr
6;324(7341):816-8.
McHaffie HE, Fowlie PW, Hume R, Laing IA, Lloyd DJ, Lyon AJ. Consent
to autopsy for neonates. Arch Dis Child Fetal Neonatal Ed. 2001 Jul;85(1):F4-7.
Department of Health. The 11th Report of the Perinatal and
Infant Mortality Committee of Western Australia 2000-01. Perth; 2002 Contract
No.: Document Number|.
Duley LM. A validation of underlying cause of death, as recorded by
clinicians on stillbirth and neonatal death certificates. Br J Obstet Gynaecol.
1986 Dec;93(12):1233-5.
Kirby RS. The coding of underlying cause of death from fetal
death certificates: issues and policy considerations. Am J Public Health. 1993
Aug;83(8):1088-91.
Sington JD, Cottrell BJ. Analysis of the sensitivity of death
certificates in 440 hospital deaths: a comparison with necropsy findings. J
Clin Pathol. 2002 Jul;55(7):499-502.
Royal College of Pathologists. Guidelines on autopsy practice: Report
of a working group of the Royal College of Pathologists. London: Royal College
of Pathologists; 2002 [updated 2002; cited 2004]; Available from:
http://www.rcpath.org/activities/publications/autopsy_practice_sept2002.html.
Hull MJ, Nazarian RM, Wheeler AE, Black-Schaffer WS, Mark EJ. Resident
physician opinions on autopsy importance and procurement. Hum Pathol. 2007
Feb;38(2):342-50.
The Royal College of Pathologists of Australasia Autopsy Working
Party. The decline of the hospital autopsy: a safety and quality issue for
healthcare in Australia. Med J Aust. 2004 Mar 15;180(6):281-5.
Rushton DI. West Midlands perinatal mortality survey, 1987. An audit
of 300 perinatal autopsies. Br J Obstet Gynaecol. 1991 Jul;98(7):624-7.
Royal College of Pathologists. Guidelines for post mortem
reports. London: Royal College of Pathologists; 2004 Contract No.: Document
Number|.
Queensland Maternal and Perinatal Quality Council. Maternal and
perinatal mortality audit: Guidelines for maternity hospitals. Queensland:
Queensland Government, Queensland Health; 2003 Contract No.: Document Number|.
Plea for Tassie's tragic babies. MERCURY. 2006 July 23.
http://www.news.com.au/mercury/story/0,22884,19878221-921,00.html.
Khong TY, Turnbull D, Staples A. Provider attitudes about gaining
consent for perinatal autopsy. Obstet Gynecol. 2001 Jun;97(6):994-8.
Khong TY, Mansor FA, Staples AJ. Are perinatal autopsy rates
satisfactory? Med J Aust. 1995;162(9):469-70.
Royal College of Pathologists of Australasia. The decline of the
hospital autopsy: a safety and quality issue for healthcare in Australia. Med J
Aust. 2004 Mar 15;180(6):281-5.
AHMAC Subcommittee on Autopsy Practice. The national code of ethical
autopsy practice. Adelaide: SA Department of Human Services; 2002 5 April
Contract No.: Document Number|.
Khong TY. Improving perinatal autopsy rates: who is counseling
bereaved parents for autopsy consent? Birth. 1997 Mar;24(1):55-7.
VanMarter LJ, Taylor F, Epstein MF. Parental and physician-related
determinants of consent for neonatal autopsy. Am J Dis Child. 1987
Feb;141(2):149-53.
Khong TY, Arbuckle
SM. Perinatal pathology in Australia after Alder Hey. J Paediatr Child Health.
2002 Aug;38(4):409-11.
Perlman B, Freedman J, Abramovitch R, Whyte H, Kirplalani H, Perlman
M. Information needs of parents of sick neonates. Pediatrics. 1991;88:512-18.
Gardner JM. Perinatal death: uncovering the needs of midwives and
nurses and exploring helpful interventions in the United States, England, and
Japan. J Transcult Nurs. 1999 Apr;10(2):120-30.
Toedter L, Lasker J, Janssen H. International comparison of studies
using the perinatal grief scale: a decade of research on pregnancy loss. Death
Stud. 2001 April;25(3):205-28.
Murray J, Callan VJ. Predicting adjustment to perinatal death. Br J
Med Psychol. 1988 Sep;61 ( Pt 3):237-44.
Turton P, Hughes P, Evans CD, Fainman D. The incidence and
significance of post traumatic stress disorder in the pregnancy ager
stillbirth. British Journal of Psychiatry Supplement 2001;178(556-560).
Flenady V, Wilson T. Support for mothers, fathers and families after
perinatal death. Cochrane Database Syst Rev. 2008(1):CD000452.
Vicki Flenady, Tomasina Stacey, Liz Davis, Emma Kirkwood, Ros Richardson, Yee
Khong, Adrian Charles.
Last edited October 20th 2008.
Stillbirth rates for Indigenous women are over twice that of non-Indigenous
women.
Major risk factors for stillbirth (many of which are modifiable) are:
overweight and obesity, advanced maternal age (over 35), maternal smoking, and
primiparity. Prolonged pregnancy is also a modifiable risk factor for
antepartum stillbirth. The presence of fetal growth restriction in
approximately 40-50% of unexplained stillbirth is an important consideration
for future prevention strategies.
The main categories of stillbirth according to the Perinatal Society of
Australia Perinatal Death Classification (PSANZ-PDC) system are: for singleton
pregnancies, accounting for over 70% of stillbirths: Unexplained antepartum
death (28%); Congenital abnormality (20%); Maternal conditions (13%); and
Spontaneous preterm (10%). In multiple pregnancies (contributing 84% to the
total): Specific perinatal conditions (mainly twin-twin transfusion) (35%);
Spontaneous preterm (24%); Unexplained antepartum death (15%); and Congenital
abnormality (11%).
It is estimated that unexplained stillbirth is now 10 times that of SIDS 500
unexplained stillbirths each year compared to 50 SIDS deaths. The high
proportion of unexplained stillbirth is a major barrier to further reduction in
the rates of stillbirth. The lack of diagnosis leaves little clues for parents
and care providers struggling with decisions about future pregnancies.
Many stillbirths are not fully investigated and therefore important factors to
further understand why the baby died may be missed. The recommended
investigations within the PSANZ stillbirth protocol should be followed in all
cases of stillbirth. Exclusion of the presence of infection is an important
component of this protocol.
Autopsy and placental pathological examination remain the gold standard
investigation for stillbirth. Parents who have a stillborn baby should be
offered the option of an autopsy and given sufficient information (both written
and oral) to enable them to make the decision which is right for them.
Stillbirth is devastating for families and one which is often accompanied by
long lasting grief and loss of normal family functioning; the psychosocial
burden of stillbirth to the family and the broader community should not be
underestimated. While high level evidence on the best model of support for
parents following a perinatal death is lacking, maternity hospitals need to
ensure that mechanisms (including training and support for clinical staff and
processes to ensure optimal transition to community support) are put in place
to meet the individual needs of parents and families.
In Australia for the year 2011, based on data from the National Perinatal
Statistics Unit derived from State and Territory perinatal data collections (3)
there were 301,810 births, and 2,992 perinatal deaths giving a perinatal
mortality rate (PMR) of 9.9 per 1000 births. The perinatal mortality comprised
of 2,220 fetal deaths, giving a fetal death rate (FDR) of 7.4 per 1000 births,
and 772 neonatal deaths, giving a neonatal death rate (NDR) of 2.6 per 1000
livebirths (of 299,588 total livebirths). The PMR of babies born to Aboriginal or Torres Strait Islander
mothers remains almost twice that of babies born to other mothers (18.6 versus
9.4) (3).
In New Zealand in 2004, there were 58,723 births and 666 perinatal deaths,
giving a PMR of 11.2 per 1000 (8.5 and 3.4/1000 for fetal and neonatal death
rates respectively) (4).
Differences in definitions and reporting processes across regions within
Australia and New Zealand (ANZ) make comparisons of perinatal mortality rates
difficult, and it is hoped that these differences will be addressed by the
various reporting agencies. The NPSU report Australias Mothers and Babies also
included the PMR for Australia calculated according to the Australian Bureau of
Statistics (ABS) which is based on death certificate data for the same year.
This rate was reported as 8.5 per 1000 (FDR 5.4, NDR 3.1). This difference is
thought to be due to the differences in definition and reporting processes by
the two sources with better ascertainment achieved by the perinatal data
collections. At a round table meeting of ANZSA and NPSU in November 2007 a
decision was made to include only stillbirth rates derived from the perinatal
collections in the annual NPSU report Australias Mothers and Babies.
According to ABS data, the PMR in Australia declined by nearly two-thirds over
the period from 1973 - 2000 from 23 per 1000 to the current rate of
approximately 8 per 1000 (5). The fall in the neonatal death component (a 75%
reduction from 12.6 to 3 per 1000) was greater than the fetal death reduction
which fell by 50% from 11 to 5 per 1000 births. Fetal death after the onset of
labour has decreased by two-thirds. Antepartum deaths decreased to a lesser
extent (46%) (5) and currently make up approximately 65% of all fetal deaths (6).
These patterns are similar to developed countries and have resulted in a focus
of attention towards reducing the antepartum stillbirth rate.
While different classifications systems make comparisons of the causes of
stillbirth across and within countries difficult, the main reported causes of
stillbirth internationally currently include: congenital abnormality,
abruption, hypertension, diabetes and other maternal conditions, and
maternal/fetal infection (8).
In approximately 30-50% of stillbirths, a cause of death is not identified (8,
13-15).
Data from a current ANZSA NHMRC funded study of 3,500 stillbirths over the
period 2000-2003 in three States of Australia (Queensland, Victoria and Western
Australia) demonstrates the main causes of death in an Australian
population (15). In this large study, according to the Perinatal Society of
Australia Perinatal Death Classification (PSANZ-PDC), the four major categories
of stillbirth in singleton pregnancies, accounting for over 70% of stillbirths,
were: Unexplained antepartum death (28%); Congenital abnormality (20%);
Maternal conditions (13%); and Spontaneous preterm (10%). In multiple
preganancies the main categories (contributing 84% to the total) were: Specific
perinatal conditions (mainly twin-twin transfusion) (35%); Spontaneous preterm
(24%); Unexplained antepartum death (15%); and Congenital abnormality
(11%) (15).
Infection is acknowledged as an important contributor to stillbirth even when
clinical markers for infection may not exist (16, 17). Although there are
increasing research data to support the importance of infection in stillbirth,
due to the lack of routine investigation for infection in many stillbirths, the
magnitude of the contribution of infection is currently not well understood (16)
and very few stillbirths in Australia are currently attributed to infection.
In pregnancy, thrombophilic disorders are associated with an increased risk of
venous thromboembolism (VTE), pre-eclampsia, placental abruption, early and
late fetal demise, recurrent pregnancy loss and fetal growth restriction (18,
19). While there is limited data on the strength of the association between
inherited thrombophilic disorders and adverse pregnancy outcome such as
stillbirth and controversy remains, recent reviews have demonstrated a
statistically significant increase in the risk of stillbirth associated with:
APC resistance(18, 20); Factor V Leiden mutation (18, 20-22); Protein C
deficiency(20); Protein S deficiency (18, 20, 21); Prothrombin G20210
mutation (20, 21); and MTHFR (20). One review also demonstrated statistically
significant associations with these thrombophilic conditions and pre-eclampsia
which was strengthened in the analysis for severe pre-eclampsia (20). Maternal thrombophilic disorders are a potentially important cause of stillbirth and, as
investigation for these conditions are often not routinely performed, it may be
responsible for a proportion of unexplained stillbirth. Ideally the
identification of thrombophilia following an apparently unexplained stillbirth
would result in intervention in future pregnancies to reduce the risk (23).
Risk factors for stillbirth include: smoking, obesity, advanced maternal age (over 35) and primparity
emerged as the most important risk factors for stillbirth (2). Prolonged
pregnancy is also a modifiable risk factor for antepartum stillbirth, which
affects about 1 per 1000 on-going pregnancies at 41 weeks, 1 in 500 at 42 weeks
and 1 in 200 at 43 weeks. These risks can be avoided by routine induction
post-dates (2).
Other reported factors which may increase the risk of stillbirth include:
previous miscarriage,stillbirth or perinatal death and previous caesarean
section (2), lower socioeconomic status (SES), alcohol and drug use (8, 24). In
the USA, black women are at increased risk of stillbirth (8), as are Indigenous
women in Australia where the risk is over twice that of non-Indigenous
women (25).
Contributing factors relating to care (also called sub-optimal, avoidable or
suspected preventable factors) have been reported in approximately 30-50% of
perinatal deaths and therefore also require consideration as part of routine
review of perinatal deaths by hospital committees. The report of the inquiry
into Obstetrics and Gynaecology Services at the King Edward Memorial
Hospital (26) highlighted the importance of clinical audit of perinatal deaths
as part of ongoing clinical practice improvement.
Reduced fetal movements and
stillbirth
Regular fetal movement is widely accepted as a sign of fetal wellbeing.
Almost all pregnant women perceive fetal movements and engage in self-screening
by reporting their concerns of decreased fetal movements (DFM). Maternal
reporting of DFM is a common pregnancy phenomenon occurring in between 4 - 15
percent of pregnancies in the third trimester . Pregnancies in which the woman
consistently reports regular fetal movements have very low morbidity and
mortality and conversely those with maternal reporting of DFM have been
associated with stillbirth, fetal growth restriction, fetal distress, preterm
birth, oligohydramnios and fetal abnormality mainly affecting the neurological
or musculoskeletal system (27)
Fetal movement monitoring has been proposed as a screening tool to detect
pregnancies at increased risk of late gestation sudden unexpected fetal death.
This proposition is supported by the observation that as many as 50% of women
perceive a gradual reduction of fetal movements several days before an
intrauterine death (28-31).
However, there is little agreement as to what constitutes normal fetal
movements (32-34) and the best methods for detection and management of a fetus
at risk on the basis of DFM remains controversial (33). The use of maternal
perception of DFM as screening tool is further complicated by the wide
variation in the amount of fetal movements perceived by the women with reports
ranging from 4-94% of movements identified by ultrasound.
In the late 1970s and early 1980s, formal fetal movement counting, which
involves providing instructions to the woman about how to count and record
movements, was a routine part of antenatal care in many settings. This practice
reduced dramatically following the report, in 1989, of the single randomised
controlled trial which concluded that formal monitoring of fetal movements did
not reduce antepartum stillbirths and placed an increased burden on hospital
resources (35). Current guidelines in the United Kingdom, the US or Norway do
not recommended formal fetal movement counting. However, this remains somewhat
controversial and others continue to recommend fetal movement counting as a
part of routine antenatal care (28, 36, 37).
The NICE Guidelines in the UK, while not supporting formal fetal movement
counting, do recommend that all women reporting DFM should be assessed for
fetal wellbeing. However, no guidance is provided on what constitutes
appropriate assessment. There is currently no randomised controlled trials
evidence on any aspect of the initial evaluation or further management of
pregnancies with decreased fetal movements. As a consequence, wide variation in
management between populations, institutions and practitioners within single
institutions is apparent 6;9;13;16;26;27;35-37 (+ ref Heazell) (38). The
Cochrane systematic review on the topic (including the only available trial
mentioned above) acknowledges the lack of evidence to inform practice and
recommends further research to determine methods of detection of DFM and
optimal management strategies (39).
A recent survey of Obstetricians in Australia and New Zealand (40) showed wide
variation in practices in the detection and management of women with decreased
fetal movement reflecting clinical uncertainty which stems from the current
lack of high quality evidence. Approximately 30% of responders use Kick Charts
as a part of routine care.
Data from the current NHMRC grant has revealed a UAFD rate of 2.0 per 1 000
births (15). This rate is almost ten times the current rate of Sudden Infant
Death Syndrome (SIDS) (45).
Using the number of ongoing pregnancies as the denominator, the risk of
unexplained antepartum fetal death is shown to increase in late pregnancy (2,
46). Data from our current NHMRC grant has demonstrated that the contribution
of UAFD increased after 23 weeks gestation reaching a maximum of 60% in term
singleton stillbirths (37-41 weeks) and 49% at 35-36 weeks for stillbirth in a
multiple pregnancy (47).
Several studies have been conducted both nationally and internationally to
identify risk factors for UAFD. However, due to small numbers, differing
methods including definitions and classification of fetal deaths, there is
limited agreement on the reported risk factors. Factors which have been
reported include: cigarette smoking in pregnancy, overweight or obesity (29);
advanced maternal age (29, 48); low maternal age (31); advanced maternal age
(29, 48, 49) duplicated?; primiparity and multiparity>3 (48); low socioeconomic
status (29, 31, 48, 49); subclinical infection (31, 50); fetal growth
restriction (11, 29, 49, 51, 52); sub-optimal antenatal care (11);
polyhydramnios, cord problems, antenatal fetal distress (53, 54); rural origin,
private accommodation status; higher systolic blood pressure (55); low blood
pressure (56), and previous caesarean section (57).
The presence of fetal growth restriction in approximately 40-50% of unexplained
stillbirth (13, 14) suggests the potential for prevention if these "at risk"
infants can be detected in the antenatal period where appropriate intervention
may be undertaken to reduce the risk.
Stillbirth audit and classification in Australia and New Zealand
The PSANZ-PMG has
developed clinical practice guidelines for audit of perinatal deaths (23) which
were disseminated across ANZ in 2005. The guidelines recommend comprehensive
non-selective investigations for stillbirths and detailed instructions on the
application of the clinical classification system for stillbirth and neonatal
deaths. Due to the often complex nature of causation of stillbirth, the clinico-pathological
correlation is best accomplished by discussion of a multidisciplinary team (11,
16, 23, 59-64) which includes obstetricians, paediatricians, neonatologists,
perinatal pathologists, geneticists, midwives, and neonatal nurses. Therefore,
the PSANZ guideline recommends review of all perinatal deaths by a
multidisciplinary team.
Stillbirths first became notifiable in Scotland in 1940 (65), and in 1954 the
classification developed by Sir Dugald Baird and his colleagues in Aberdeen for
the purpose of audit and surveillance was published (66). Subsequently,
numerous systems have emerged. In a recent search, we identified 33 new systems
(7, 11, 41, 42, 66-94) and a further 12 modifications of these systems (11,
95-105) for the classification of stillbirths causes and associated conditions
and/or suboptimal care
The majority were designed for both stillbirths and neonatal deaths, however
three systems have been designed specifically for stillbirths (42, 83, 88), the
remainder also included neonatal deaths and two systems included post-neonatal
deaths; one up to hospital discharge (74) and the other up to twelve months of
age (81). While it is important to analyse the causes of perinatal death
according to its components of stillbirth and neonatal death (106), a system
specifically designed to incorporate both groups enables interpretation of
differences in the rates and causation across regions arising from variation in
definition, reporting and registration practices for perinatal deaths (106).
In acknowledging the need and for a systematic approach to audit and review of
perinatal deaths in Australia and New Zealand (ANZ), PSANZ endorsed the
establishment of the Perinatal Mortality Group (PSANZ-PMG) (107) in March 2003.
In the absence of an available classification system which suited the needs of
this group, a new classification system (PSANZ Perinatal Death Classification
(PSANZ-PDC) (69) was developed based on those used in Queensland and South
Australia which were based on the Whitfield system (70).
The purpose of the classification is to determine the single most important
obstetric factor which leads to the chain of events which resulted in the death
and in doing so aims to identify avoidable stillbirth. The classification has
been shown to have a high level of clinical agreement (108) and results in
approximately 30% unexplained antepartum deaths (10) which has been suggested as
a measure for an acceptable classification system (41). In a recent evaluation
of six systems across seven countries, the PSANZ-PDC performed well (109).
Within this classification, fetal deaths prior to the onset of labour or
membrane rupture where no cause for the death was able to be determined and,
following review of all relevant available clinical information are assigned to
the category of Unexplained antepartum death. However, unlike unexplained
infant death (Sudden Infant Death Syndrome), the Unexplained antepartum death
category is not dependent on the level of investigation and does not include
the requirement for an autopsy examination. This may result in
misclassification and overestimation of the contribution of UAFD (29).
Formal protocols are intended to guide caregivers in stillbirth investigation,
to ensure the quality and consistency of the investigation which will enable
the validity of comparisons of trends across regions and over time. A recent
systematic review of protocols, or component of protocols, for determining the
causes of stillbirth by Corabian and Scott (110) identified five formal
protocols currently in use, including the PSANZ stillbirth protocol (23). A
comparison of the components of these protocols has identified some variation.
However, all protocols recommended placental pathology and autopsy. In the
review of individual studies to determine appropriate investigations, the
authors identified 53 studies potentially meeting the inclusion criteria. Of
these, 46 were excluded due to lack of information in the published reports to
adequately assess eligibility, poor methodological quality, or the definition
of stillbirths which did not meet the inclusion criteria, leaving seven
included studies (111-117). All included studies evaluated autopsy and
placental pathology.
The results confirmed the value of these investigations. In the five
retrospective studies (113-115, 117, 118) autopsy findings were shown to:
confirm clinical findings in 29% to 89% of cases; change the diagnosis in 10%
to 38%; and provide additional information in 4 to 24%. Despite this, the cause
of death remained unexplained in up to 40% of stillbirths. In the two
prospective studies (111, 116) placental pathology was shown to confirm clinical
or autopsy findings or both in up to 75% of cases and were diagnostic in 23% to
46%.
The authors of this review concluded that, while autopsy and placental
pathology were valuable, due to a lack of high quality data on the value of
other investigations, "no formal scientific judgement could be made on which is
the most appropriate protocol for stillbirth investigations or which components
should be considered for the most relevant and efficient investigative
protocol"(110).
Despite methodological concerns raised by Corabian and Scott, in recent years
several studies on stillbirth protocols have consistently demonstrated that
sufficient valuable information is obtained to justify the use of comprehensive
investigation protocols (9, 61, 114, 119-123). While results for individual
components of the investigation protocols across studies are conflicting, all
studies have reported that formal protocols provide useful information (either
a cause of death or additional valuable information for future pregnancy
counselling) in approximately 30-50% of stillbirths.
However, these studies also report a substantial proportion of stillbirths
remaining unexplained, ranging from 60% (61) to 36% (124). Differences in the
components of the protocols, definition of stillbirth, the classification
systems, and study design (population or hospital based) render comparisons and
interpretation of the findings of these studies problematic. The two largest
studies to date come from the Wisconsin Stillbirth Surveillance Program (61) and Incerpi et al (124). The WiSSP is a regional referral program for investigation
of stillbirth which has reported prospectively collected population based data
study on investigation and causes of death in over 1000 stillbirths (defined as
gestation >20 weeks or over 375gms birthweight). This series has shown that
using a non-selective approach to the investigation of fetal causes of death
improved the yield of helpful information in 50% of stillbirths. The
investigators reported that all individual components of the protocol yielded
critical information, whereby exclusion of any single component would result in
missed diagnoses in 2% (family history) to 15% (autopsy and placental
pathology) of cases. However, the focus of the WiSSP protocol is fetal
investigation and the extent to which maternal investigation (eg for infection,
or other medical conditions) is undertaken is unclear apart from the Kleihauer-Betke
test for maternal-fetal haemorrhage.
The other study (124), a retrospective study of over 700 stillbirths at a single
institution, showed that while the use of a comprehensive protocol resulted in
a high yield from autopsy and placental pathology, other investigations
including the Kleihauer-Betke and maternal screening for congenital infection
was low. The finding of low yield for the Kleihauer-Betke test is in conflict
with other reports (122, 125). The overall autopsy rate in this series was 60%,
and the proportion of unexplained stillbirth was 36%. A lower number of
unexplained fetal deaths was reported for stillbirths with an autopsy than
those without (31% v 44%). A hospital based study by Lim et al examined the
value of a selective approach to investigation based on the presence of certain
obvious causes of death (123). In this small series of 55 stillbirths with an
autopsy rate of only 28%, the investigators reported that 38% of cases remained
unexplained, similar to that of the non-selective approach.
There is currently no
available data on the value of either a selective or non-selective protocol for
investigation of stillbirths in an Australian setting. A large-scale prospective study is currently under way across hospitals in Australia and New Zealand. See 'ANZSA Investigating Causes of Stillbirth: a prospective cohort study examining use and effectiveness of a comprehensive investigation protocol' on our Research Projects page.
The PSANZ guidelines recommend a comprehensive non-selective stillbirth
investigation protocol. While it is acknowledged that compliance with the
protocol may depend on the particular circumstances of the death (e.g. family
wishes and access to services), using a selective investigative approach may
result in missed important diagnoses (61), therefore the guideline recommends
that clinicians adopt the non-selective approach as the standard and debate the
relative merits of not following this approach on an individual case basis.
Unfortunately, due to a lack of information about the value of many of the
recommend investigations, these investigations are largely based on consensus
of the guideline development working party and not evidence. As a result, there
is some clinical controversy about the recommendations and unwillingness by
clinicians to follow the recommendations. Further research is urgently need to
determine the best approach to investigation of stillbirth.
Investigation of
stillbirth in Australia
While no information is available on the yield of investigations for stillbirth
in ANZ, preliminary data from the current ongoing NHMRC study on almost 200
stillbirths provides some indication of current practices in investigation. In
three states of Australia over the period 2000-2003 (pre dissemination of the
PSANZ guidelines), a low rate for a number of the currently recommended core
investigation for stillbirths is evident as follows: autopsy 45% (54% for
unexplained stillbirths); placental histopathology 45%; vaginal cultures 5%;
amniocentesis for culture <1%, amniocentesis for chromosomal analysis <2%;
Kleihauer-Betke 60%; external examination of the baby by clinician 60%;
Clinical photographs 30%; Glycosolated haemoglobin (HBA1c) 40%; maternal full
blood count and blood group and antibodies 75%, thrombophilia screening 20%
(126). The extent to which this apparently low level of investigation is
artificially inflating the number of unexplained stillbirths in Australia is
not known.
Costs of stillbirth
investigations
There is very limited information currently available to enable consideration
of the cost benefit of stillbirth investigation protocols, or their individual
components. Michalski et al (120) reported a cost consequence analysis from the
Wisconsin Stillbirth Service Program (WiSSP) (61) which showed the real cost of
a comprehensive stillbirth protocol was $1450USD per assessment or
approximately $12USD per cared-for pregnancy. In this series of almost 1500
stillbirths, new relevant information was identified in 51% of stillbirths as a
result of the protocol. The authors concluded that the comprehensive protocol
should become a part of routine antenatal care. Another study (123) estimated
that a selective approach to investigation of stillbirths would reduce the
costs of investigation in 30% of cases without compromising the yield of
investigation. There is currently no data available on costs to enable
consideration of the cost benefit of stillbirth investigations in an Australian
or New Zealand setting.
The autopsy examination is the gold standard for identification of the cause of
perinatal death (127); diagnostic utility of the perinatal autopsy has been
repeatedly demonstrated (128). One comprehensive review of 27 studies found
perinatal autopsy to change diagnosis or provide additional findings in 22-76%
of cases (128). In another review of 53 studies across a range of health care
settings, diagnostic errors detected at perinatal autopsy showed a median error
rate in pre-autopsy diagnosis of 23.5% for major errors (clinically missed
diagnoses involving a principal underlying disease or primary cause of death)
and 9% for Class 1 errors (major error that, had they been detected during
life, "would", "could", "possibly" or "might" have affected patient prognosis
or outcome).
The recent systematic review of stillbirth investigations (110) found that while
the evidence base for many recommended investigations is in doubt, autopsy and
placental pathology make a valuable diagnostic contribution. The reviewers
concluded that data derived from the review may be "helpful in counselling
parents who are considering the difficult decision of whether or not to consent
to a post-mortem examination following a stillbirth" (110). In addition to the
value of information obtained at autopsy in the planning and management of
future pregnancies (129) autopsy may have long-term psychological implications
for parents. Parents, mothers in particular, often attribute the death of their
child to their own actions (130, 131). Autopsy findings may give reassurance
that they are not to blame and assist in grief integation (130). Some parents
may regret the decision to have an autopsy, particularly when no cause of death
is identified, and some may find comfort in an altruistic perspective where no
cause is found after autopsy examination (131).
A study in WA by Dr Buccilli and Charles confirmed the findings of the value of
the perinatal autopsy in an Australian context (132). In this study, a total 98
of the 167 stillbirths (58.7%) had an autopsy performed. Examination of the
quality of autopsy, using a modified scoring system (117), revealed that in 25%
the autopsy confirmed clinical diagnoses; in 21% the autopsy findings changed
the diagnosis; in 31% some extra information to the original diagnosis was
identified; and in 23% the findings were inconclusive. A more recent study from
Western Australia of 1619 fetal deaths revealed 49% having had complete autopsy
investigation. Following autopsy 22% of these deaths were explained and a
further 18% were identified as having fetal growth restriction. In addition, of
the 42% of deaths which were unexplained on the death certificate, 65% were
explained after autopsy investigation (44). Based on these findings, it is
evident that the cause of death recorded on perinatal death certificates
without an autopsy are often misleading and therefore may jeopardise the
quality of research and audit activities and subsequent public health policy
based on these data (118, 133-135).
Perinatal autopsy is important for education, training and to ensure high
standards in perinatal pathology (136-138)
There is limited research on the quality of perinatal autopsies however, the
available data suggests that approximately half may not reach minimum
standards (62, 139). The post-mortem examination of an infant is very different
to that performed on an adult (8, 16, 63, 64), and ideally should be performed
by a paediatric pathologist. Pathologists with paediatric training find a
higher incidence of causes of death in infants (112) and provide a much higher
proportion of adequate reports (139, 140). The Confidential Enquiry into
Stillbirth and Deaths in Infancy (CESDI) in the United Kingdom have reported
that the causes of death based on perinatal/paediatric pathologists reports are
infrequently revised (11). Cartlidge et al demonstrated an association with
higher quality autopsy and the number of perinatal and infant deaths where the
main cause of death was identified (112). Understandably, the ethics of
approaching parents for consent where a quality post-mortem service is not
available has been questioned (127). There are currently no guidelines for ANZ
on quality and minimum standards for perinatal autopsies.
Decline in autopsy rates
An optimal perinatal autopsy rate of 75% is recommended by the Royal College of
Pathologists (136). However, the perinatal autopsy rate has steadily declined
over recent years in many regions. Perinatal autopsy rates vary across
jurisdictions in Australia. The rates in our previous study across three States
in 2000 were 39%, 48% and 70% overall, and 96%, 59% and 62% for unexplained
antepartum deaths (10). In our current NHMRC funded population based study, the
overall unexplained stillbirth autopsy rate in singletons over the period
2000-2003 was 45%; consistent across the three participating states. In
Queensland, the autopsy rate for stillbirths has declined by 50% from the
period 1997-2003 to the current rate of 30% (141). The recent perinatal autopsy
rate in Tasmania was 7% (142).
Reasons for the decline
While research into the determinants of the decreasing perinatal autopsy rate
is limited, consent is considered a major factor (137, 143, 144). Adverse
publicity following the inquiries into autopsy practices in the United Kingdom
and the NSW Institute of Forensic Pathology (129) are thought to have affected
clinicians willingness to seek consent and parents acceptance of the
procedure (130). Although the inquiries led to improved practices, complexity in
the consent process also increased and this may be a deterrent to both
clinicians and parents (145). Workforce shortages in clinical care settings and
pathology are also limiting adequate autopsy rates (138).
Two surveys have examined attitudes of staff to perinatal autopsy (143, 148).
Both studies indicate that the attitudes of staff and the experience level of
staff exert important influences on consent to autopsy. The Australian survey
of staff by Khong et al (143) showed that while obstetricians and
neonatologists were not averse to seeking consent midwives and neonatal nurses
were reluctant to do so. Obstetricians and neonatologists rated nurses and
midwives as influential in parents decisions around autopsy. However,
clinicians report feeling inadequate talking to parents about autopsy, and may
avoid discussion due to compassion and their lack of confidence to provide care
following a perinatal death (137, 143). Research into parents perspectives and
experiences on perinatal autopsy is very limited. However, it does appear that
parents may regret their decision about autopsy and that this may be related to
inadequate information and communication at the time of consent (131).
Two small studies have reported the frequency of parents regret about the
decision for autopsy on their baby or infant with conflicting results (130,
131). McHaffie et al, in interviews with parents after a neonatal death,
reported that no parent expressed regret about the decision. However, in the
survey by Rankin et al (130) of 148 women after pregnancy or infant loss
(including miscarriage, termination, stillbirth, neonatal or post-neonatal
death), approximately 10% regretted their decision; more parents who had
declined an autopsy regretted the decision than parents who had agreed. This
survey also showed that 80% of parents would agree to a post-mortem examination
if asked (130). Therefore, clinician reluctance to seek consent due to
compassionate reasons may be misplaced.
Other factors which may affect clinician willingness to approach parents for
consent for paediatric and perinatal deaths include: lower gestation at
death (143, 149); discipline and seniority of clinicians (148); ambivalence about
the value of an autopsy (112); and lack of technical understanding of the
autopsy procedure. Parents enduring powerful negative experiences such as the
stillbirth of their baby may not recall information given to them (150) which
may lead to negative feelings towards care providers for poor communication
increasing parental distress. Staff need specific training to know how to
respond appropriately to bereaved parents following stillbirth (151).
The paucity of well conducted research on communication and consent for autopsy
in stillbirths does not permit reliable conclusions to be drawn. Major
limitations of the current research includes: small numbers studied; combining
the populations of stillbirths and neonatal deaths; and the use of parent
groups as the sampling frame which may result in an overestimate of negative
outcomes and experiences of parents (152). The situation of a stillbirth (often
an unexpected event in the antenatal period) differs significantly from that of
a neonatal death (often death occurs after a period of time in an intensive
care nursery). Therefore, it stands to reason that communication and
information needs of parents are quite different and each are deserving of
focused research.
Pilot data on experiences and views of parents about autopsy consent were
obtained through the consultation process to update the Perinatal Society of
Australia and New Zealand (PSANZ) Mortality Audit Guidelines. The views and
experiences of bereaved parents and their satisfaction with information
provided to them around the time of their stillbirth were gathered by
Stillbirth and Neonatal Death Support (SANDS) Queensland and the NSW Stillbirth
Foundation. Seventeen parents (14 mothers and three fathers) identified through
the SANDS newsletter and by word of mouth attended three focus groups. All
parents experienced late gestation stillbirths. The majority had consented to
an autopsy but the cause of death remained unexplained.
Parents frequently commented on their inability to make an informed decision
about autopsy due to overwhelming shock and grief and their dependence on
others in the decision making process. One parent did not understand that the
investigation was optional, and some participants stated feeling dependent on
professionals for their decision. Some parents felt it was the responsibility
of the care provider to make the decision on their behalf, comparing this to
other emergency type decisions which are made in their best interests (eg
emergency caesarean section) and felt let down by the care provider. Others
felt vulnerable due to perceptions of lack of objectivity from their care
provider, resulting from possible concerns about clinical error, and would have
preferred to discuss the option of autopsy with a third party.
The need to involve others such as their babys grandparents and friends in
interpreting information was important to parents. All agreed that written, as
well as verbal information, about an autopsy was important, but eight parents
had no recollection of receiving written information. Three parents did not
recall any conversation with their care providers about the option of autopsy.
This appeared to be influenced by presenting the decision as urgent and giving
inadequate information. Negative feelings towards autopsy included: fear of
mutilation; limiting the available time to spend with the baby; and concerns
that an autopsy could indicate some blame to the mother for "doing something
wrong". Some parents said that the autopsy, even when it did not reveal a cause
for the death, helped them in "moving forward". All parents who did not have an
autopsy expressed regret or some doubt about their decision. No parent who had
an autopsy performed expressed these feelings.
Parents frequently raised concerns about clinical staff seeming inadequate in
coping with the event of stillbirth. They commented that some staff seemed
"scared" and did not appear to have an understanding of how parents respond to
loss of a baby. Many parents suggested the need for special training of health
care providers in communicating with parents after a stillbirth. Satisfaction
with information and counselling about autopsy appeared to be related to trust
in the heath care provider and displaying compassion and understanding of what
the parents were experiencing.
Current research to inform best practise on the information needs and consent
practices for autopsy around the time of stillbirth is limited. Lack of
appropriate care may have long term consequences for bereaved parents. These
pilot data, despite being limited by possible volunteer bias, support the need
to improve care in relation to autopsy consent.
A large-scale study, which is currently being piloted, aims to identify factors
that contribute to the low autopsy consent rate for stillbirths and will
provide robust information to develop information and educational materials
that address the needs of parents and clinicians.
Acknowledgment: We wish to acknowledge the parents who participated in the
focus groups.
The death of an infant is among the most stressful of life events (153) and
bereaved parents may experience acute emotional distress (153). Initial
responses to an infants death include numbness, confusion, depersonalisation
and disbelief and shock. This may be an adaptive mechanism to temporarily
protect parents from the full impact of their babys death, however, mothers
may continue to experience feelings of depersonalisation up to four years
later (153). Bereaved fathers may deny the emotional impact of the
experience (153), with up to 10% exhibiting "almost complete denial". Symptoms
of depression may also continue for two years or more (153).
While grief after a stillbirth is a normal reaction, recent research has
suggested that stillbirth may be associated with Post Traumatic Distress
Disorder (PTSD) (154). Factors which have been reported to increase the risk of
adverse psychological outcomes for parents after a perinatal death include:
perceived inadequate social support, traumatic circumstances surrounding the
death, difficulties in coping with a crisis in the past, problematic
relationships in the nuclear family and the presence of other life crises. In
addition, mothers report greater distress than do fathers.
A recent Cochrane review on support interventions for families after a
perinatal death (155) concluded that there is insufficient evidence from
randomised controlled trials to provide reliable information on which to base
practice. While providing support for parents and families after a perinatal
death is justified based on other types of research, there is insufficient
evidence to confirm or refute the benefit of the different types of
interventions aiming to provide such support.
This overview was initially prepared by :
Vicki Flenady, Tomasina Stacey, Liz Davis, Ros Richardson, Yee Khong, Adrian
Charles.
Last edited October 20th 2008.