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Licensed Unlicensed Requires Authentication Published by De Gruyter February 24, 2016

Classification of stillbirths is an ongoing dilemma

  • Luigi Nappi , Federica Trezza , Pantaleo Bufo , Irene Riezzo , Emanuela Turillazzi , Chiara Borghi EMAIL logo , Gloria Bonaccorsi , Gennaro Scutiero , Vittorio Fineschi and Pantaleo Greco



To compare different classification systems in a cohort of stillbirths undergoing a comprehensive workup; to establish whether a particular classification system is most suitable and useful in determining cause of death, purporting the lowest percentage of unexplained death.


Cases of stillbirth at gestational age 22–41 weeks occurring at the Department of Gynecology and Obstetrics of Foggia University during a 4 year period were collected. The World Health Organization (WHO) diagnosis of stillbirth was used. All the data collection was based on the recommendations of an Italian diagnostic workup for stillbirth. Two expert obstetricians reviewed all cases and classified causes according to five classification systems.


Relevant Condition at Death (ReCoDe) and Causes Of Death and Associated Conditions (CODAC) classification systems performed best in retaining information. The ReCoDe system provided the lowest rate of unexplained stillbirth (14%) compared to de Galan-Roosen (16%), CODAC (16%), Tulip (18%), Wigglesworth (62%).


Classification of stillbirth is influenced by the multiplicity of possible causes and factors related to fetal death. Fetal autopsy, placental histology and cytogenetic analysis are strongly recommended to have a complete diagnostic evaluation. Commonly employed classification systems performed differently in our experience, the most satisfactory being the ReCoDe. Given the rate of “unexplained” cases, none can be considered optimal and further efforts are necessary to work out a clinically useful system.

Corresponding author: Chiara Borghi, Institute of Obstetrics and Gynecology, Department of Morphology, Surgery and Experimental Medicine, University of Ferrara, Ferrara, Italy, E-mail:


[1] World Health Organization. Neonatal and perinatal mortality: country, regional and global estimates. WHO Libr Cat Data, 2006. Available at in Google Scholar

[2] Gordon A, Raynes-Greenow C, McGeechan K, Morris J, Jeffery H. Risk factors for antepartum stillbirth and the influence of maternal age in New South Wales Australia: a population based study. BMC Pregnancy Childbirth. 2013;13:12.10.1186/1471-2393-13-12Search in Google Scholar

[3] Reddy UM, Goldenberg R, Silver R, Smith GC, Pauli RM, Wapner RJ, et al. Stillbirth classification – developing an international consensus for research: executive summary of a National Institute of Child Health and Human Development Workshop. Obs Gynecol. 2009;114:901–14.10.1097/AOG.0b013e3181b8f6e4Search in Google Scholar

[4] King JF, Warren RA. The role of reviews of perinatal deaths. Semin Fetal Neonatal Med. 2006;11:79–87.10.1016/j.siny.2005.11.008Search in Google Scholar

[5] Flenady V, Frøen JF, Pinar H, Torabi R, Saastad E, Guyon G, et al. An evaluation of classification systems for stillbirth. BMC Pregnancy Childbirth. 2009;9:24.10.1186/1471-2393-9-24Search in Google Scholar

[6] Wigglesworth JS. Monitoring perinatal mortality. Lancet. 1980;ii:684–6.10.1016/S0140-6736(80)92717-8Search in Google Scholar

[7] 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;103:30–6.10.1016/S0301-2115(02)00023-4Search in Google Scholar

[8] Gardosi J, Kady SM, McGeown P, Francis A, Tonks A. Classification of stillbirth by relevant condition at death (ReCoDe): population based cohort study. Br Med J. 2005;331:1113–7.10.1136/bmj.38629.587639.7CSearch in Google Scholar PubMed PubMed Central

[9] Korteweg FJ, Gordijn SJ, Timmer A, Erwich JJ, Bergman KA, Bouman K, et al. The Tulip classification of perinatal mortality: Introduction and multidisciplinary inter-rater agreement. Br J Obstet Gynaecol. 2006;113:393–401.10.1111/j.1471-0528.2006.00881.xSearch in Google Scholar PubMed

[10] Frøen JF, Pinar H, Flenady V, Bahrin S, Charles A, Chauke L, et al. Causes of death and associated conditions (Codac): a utilitarian approach to the classification of perinatal deaths. BMC Pregnancy Childbirth. 2009;9:22.10.1186/1471-2393-9-22Search in Google Scholar PubMed PubMed Central

[11] Facchinetti F, Reddy U, Stray-Pedersen B, Baronciani D, Requejo JH. Stillbirth International Group. International issues in stillbirth. J Matern Fetal Neonatal Med. 2008;21:425–8.10.1080/14767050802040849Search in Google Scholar PubMed

[12] Facchinetti F, Alberico S, Benedetto C, Cetin I, Cozzolino S, Di Renzo GC, et al. A multicenter, case-control study on risk factors for antepartum stillbirth. J Matern Fetal Neonatal Med. 2011;24:407–10.10.3109/14767058.2010.496880Search in Google Scholar PubMed

[13] Siebert JR. Perinatal, fetal and embryonic autopsy. In: Gilbert- Barness E, editor. Potter’s pathology of the fetus, infant and child, 2nd edition. Philadelphia, PA: Elsevier; 2007. p. 695–740.Search in Google Scholar

[14] Vergani P, Cozzolino S, Pozzi E, Cuttin MS, Greco M, Ornaghi S, et al. Identifying the causes of stillbirth: a comparison of four classification systems. Am J Obstet Gynecol. 2008;99:319.e1–319.e4.10.1016/j.ajog.2008.06.098Search in Google Scholar PubMed

[15] Korteweg FJ, Erwich JJ, Timmer A, van der Meer J, Ravisé JM, Veeger NJ, et al. Evaluation of 1025 fetal deaths: proposed diagnostic workup. Am J Obstet Gynecol. 2012;206:53.e1–53.e12.10.1016/j.ajog.2011.10.026Search in Google Scholar PubMed

[16] Serena C, Marchetti G, Rambaldi MP, Ottanelli S, Di Tommaso M, Avagliano L, et al. Stillbirth and fetal growth restriction. J Matern Fetal Neonatal Med. 2013;26:16–20.10.3109/14767058.2012.718389Search in Google Scholar PubMed

[17] Ofir K, Kalter A, Moran O, Sivan E, Schiff E, Simchen MJ. Subsequent pregnancy after stillbirth: obstetrical and medical risks. J Perinat Med. 2013;41:543–8.10.1515/jpm-2013-0013Search in Google Scholar PubMed

[18] Gordijn SJ, Korteweg FJ, Erwich JJ, Holm JP, van Diem MT, Bergman KA, et al. A multilayered approach for the analysis of perinatal mortality using different classification systems. Eur J Obstet Gynecol Reprod Biol. 2009;144:99–104.10.1016/j.ejogrb.2009.01.012Search in Google Scholar PubMed

[19] Wigglesworth JS. Classification of perinatal deaths. Soz Praventivmed. 1994;39:11–4.10.1007/BF01369938Search in Google Scholar PubMed

[20] Burke CJ, Tannenberg AE. Intrapartum stillbirths in hospital unrelated to uteroplacental vascular insufficiency. Pediatr Dev Pathol. 2007;10:35–40.10.2350/06-02-0042.1Search in Google Scholar PubMed

[21] Korteweg FJ, Gordijn SJ, Timmer A, Holm JP, Ravisé JM, Erwich JJ. A placental cause of intra-uterine fetal death depends on the perinatal mortality classification system used. Placenta. 2008;29:71–80.10.1016/j.placenta.2007.07.003Search in Google Scholar PubMed

[22] Amir H, Weintraub A, Aricha-Tamir B, Apel-Sarid L, Holcberg G, Shiner E. A piece in the puzzle of intrauterine fetal death: pathological findings in placentas from term and preterm intrauterine fetal death pregnancies. J Matern Fetal Neonatal Med. 2009;22:759–64.10.3109/14767050902929396Search in Google Scholar PubMed

[23] Pinar H, Goldenberg RL, Koch MA, Heim-Hall J, Hawkins HK, Shehata B, et al. Placental findings in singleton stillbirths. Obstet Gynecol. 2014;123(2 Pt 1):325–36.10.1097/AOG.0000000000000100Search in Google Scholar PubMed PubMed Central

[24] Reggiani Bonetti L, Ferrari P, Trani N, Maccio L, Schirosi L, Sartori G, et al. The role of fetal autopsy and placental examination in the causes of fetal death: a retrospective study of 132 cases of stillbirths. Arch Gynecol Obstet. 2011;283:231–41.10.1007/s00404-009-1317-4Search in Google Scholar PubMed

[25] Silver RM, Varner MW, Reddy U, Goldenberg R, Pinar H, Conway D, et al. Work-up of stillbirth: a review of the evidence. Am J Obs Gynecol. 2007;196:433–44.10.1016/j.ajog.2006.11.041Search in Google Scholar PubMed PubMed Central

[26] Conti N, Torricelli M, Voltolini C, Vannuccini S, Clifton VL, Bloise E, et al. Term histologic chorioamnionitis: a heterogeneous condition. Eur J Obstet Gynecol Reprod Biol. 2015;188:34–8.10.1016/j.ejogrb.2015.02.034Search in Google Scholar PubMed

[27] Gordon A, Lahra M, Raynes-Greenow C, Jeffery H. Histological chorioamnionitis is increased at extremes of gestation in stillbirth: A population-based study. Infect Dis Obstet Gynecol. Vol. 2011, Article ID 456728, 7 pages, 2011.10.1155/2011/456728Search in Google Scholar PubMed PubMed Central

[28] Bukowski R, Hansen NI, Willinger M, Willinger M, Reddy UM, Parker CB, et al. Fetal growth and risk of stillbirth: a population-based case-control study. PLoS Med. 2014;11:e1001633.10.1371/journal.pmed.1001633Search in Google Scholar PubMed PubMed Central

[29] Bukowski R. Stillbirth and fetal growth restriction. Clin Obstet Gynecol. 2010;53:673–80.10.1097/GRF.0b013e3181eba0dbSearch in Google Scholar PubMed

[30] Gardosi J, Madurasinghe V, Williams M, Malik A, Francis A. Maternal and fetal risk factors for stillbirth: population based study. Br Med J. 2013;346:f108.10.1097/OGX.0b013e31829183a7Search in Google Scholar

[31] The Stillbirth Collaborative Research Network Writing Group. Causes of death among stillbirths. J Am Med Assoc. 2011;306:2459–68.10.1001/jama.2011.1823Search in Google Scholar PubMed PubMed Central

[32] VanderWielen B, Zaleski C, Cold C, McPherson E. Wisconsin stillbirth services program: A multifocal approach to stillbirth analysis. Am J Med Genet Part A. 2011;155:1073–80.10.1002/ajmg.a.34016Search in Google Scholar PubMed

[33] Helgadõttir LB, Turowski G, Skjeldestad FE, Jacobsen AF, Sandset PM, Roald B, et al. Classification of stillbirths and risk factors by cause of death. A case-control study. Acta Obstet Gynecol Scand. 2013;92:325–33.10.1111/aogs.12044Search in Google Scholar PubMed

  1. The authors stated that there are no conflicts of interest regarding the publication of this article.

Received: 2015-9-13
Accepted: 2016-1-18
Published Online: 2016-2-24
Published in Print: 2016-10-1

©2016 Walter de Gruyter GmbH, Berlin/Boston

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