A multidisciplinary and structured investigation of three suspected clusters of transverse upper limb reduction defects in France.

Birth defects Cluster Congenital anomalies Environment Limb reduction defects Spatiotemporal analyses

Journal

European journal of epidemiology

ISSN: 1573-7284

Titre abrégé: Eur J Epidemiol

Pays: Netherlands

ID NLM: 8508062

Informations de publication

Date de publication:
27 Apr 2024

Historique:

received: 14 11 2023

accepted: 01 04 2024

medline: 27 4 2024

pubmed: 27 4 2024

entrez: 26 4 2024

Statut: aheadofprint

Résumé

Between 2019-2021, facing public concern, a scientific expert committee (SEC) reanalysed suspected clusters of transverse upper limb reduction defects (TULRD) in three administrative areas in France, where initial investigations had not identified any risk exposure. We share here the national approach we developed for managing suspicious clusters of the same group of congenital anomalies occurring in several areas. The SEC analysed the medical records of TURLD suspected cases and performed spatiotemporal analyses on confirmed cases. If the cluster was statistically significant and included at least three cases, the SEC reviewed exposures obtained from questionnaires, environmental databases, and a survey among farmers living near to cases' homes concerning their plant product use. After case re-ascertainment, no statistically significant cluster was observed in the first administrative areas. In the second area, a cluster of four children born in two nearby towns over two years was confirmed, but as with the initial investigations, no exposure to a known risk factor explaining the number of cases in excess was identified. In the third area, a cluster including just two cases born the same year in the same town was confirmed. Our experience highlights that in the event of suspicious clusters occurring in different areas of a country, a coordinated and standardised approach should be preferred.

Identifiants

DOI: 10.1007/s10654-024-01125-5 PMID: 38671254

pubmed: 38671254

doi: 10.1007/s10654-024-01125-5

pii: 10.1007/s10654-024-01125-5

doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Informations de copyright

Références

CDC (Center for Disease Control and Prevention). Investigating suspected cancer clusters and responding to community concerns. Guidelines from CDC and the Council of State and Territorial Epidemiologists. Atlanta: CDC; 2013.

Dolk H, Loane M, Teljeur C, Densem J, Greenlees R, McCullough N, et al. Detection and investigation of temporal clusters of congenital anomaly in Europe: seven years of experience of the EUROCAT surveillance system. Eur J Epidemiol. 2015;30(11):1153–64.

pubmed: 25840712 pmcid: 4684832 doi: 10.1007/s10654-015-0012-y

Castilla E. Valproic acid and spina bifida. Lancet. 1983;2(8351):683.

pubmed: 6136822 doi: 10.1016/S0140-6736(83)92561-8

Robert E, Rosa F. Valproate and birth defects. Lancet. 1983;2(8359):1142.

pubmed: 6138672 doi: 10.1016/S0140-6736(83)90656-6

Goujard J. Clusters of birth defects: emergency and management. A review of some publications. Eur J Epidemiol. 1999;15(9):853–62.

pubmed: 10608366 doi: 10.1023/A:1007530216916

Kucik JE, Bitsko RH, Williams L, Lazarus C, Jarman DW, Correa A. Birth Defects Cluster Study: a national approach to birth defects cluster investigations. Birth Defects Res A Clin Mol Teratol. 2008;82(11):805–11.

pubmed: 18985695 doi: 10.1002/bdra.20518

Gnansia E, Michon L, Amar E, Estève J. Evidence for a cluster of rare birth defects in the Ain department (France). Birth Defects Res. 2021;113(13):1015–25.

pubmed: 33565281 doi: 10.1002/bdr2.1876

Williams LJ, Honein MA, Rasmussen SA. Methods for a public health response to birth defects clusters. Teratology. 2002;66(Suppl 1):S50–8.

pubmed: 12239745 doi: 10.1002/tera.90011

Castilla EE, Mastroiacovo P, López-Camelo JS, Saldarriaga W, Isaza C, Orioli IM. Sirenomelia and cyclopia cluster in Cali, Colombia. Am J Med Genet A. 2008;146a(20):2626–36.

pubmed: 18798307 doi: 10.1002/ajmg.a.32506

Germonneau P, Tillaut H, Dos Santos Eugenia G, Olivier B. Methodological aspects of investigating reports of spatio-temporal clusters of non-infectious diseases (Aspects méthodologiques de l’investigation des signalements d’agrégats spatio-temporels de maladies non infectieuses). Risques & Santé. 2005;4:329–34 (In French).

Santé publique France Anses. First report of the Scientific Expert Committee on transverse upper limb reduction (TULRD) (Premier rapport du Comité d’experts scientifiques sur les agénésies transverses des membres supérieurs (ATMS)). In French. 2021. Available at: https://www.santepubliquefrance.fr/maladies-et-traumatismes/maladies-de-la-mere-et-de-l-enfant/anomalies-et-malformations-congenitales/documents/note-scientifique-en-reponse-a-une-saisine/premier-rapport-sur-les-agenesies-transverses-des-membres-superieurs-atms-.-saisine-n-2018-sa-0242-demande-d-avis-relatif-a-l-existence-de-cas

Santé publique France Anses. Supplement to the report of the Scientific Expert Committee on Transverse Upper Limb Reduction published on 11 July 2019 (Complément au rapport du comité d’experts scientifiques sur les Agénésies Transverses des Membres Supérieurs publié le 11 juillet 2019. Saisine n° 2018-SA-0242 « Demande d’avis relatif à l’existence de cas groupés d’agénésie transverse des membres supérieurs dans des zones géographiques restreintes de trois départements (Ain, Morbihan et Loire-Atlantique) ». In French. 2021. Available at: https://www.santepubliquefrance.fr/maladies-et-traumatismes/maladies-de-la-mere-et-de-l-enfant/anomalies-et-malformations-congenitales/documents/rapport-synthese/complement-au-rapport-du-comite-d-experts-scientifiques-sur-les-agenesies-transverses-des-membres-superieurs-atms-publie-le-11-juillet-2019.-sai

Wynne JW, Program CBDM. Investigating birth defects clusters: a systematic approach: the program; 1993.

Bermejo-Sánchez E, Posada de la Paz M. Congenital anomalies: cluster detection and investigation. Adv Exp Med Biol. 2017;1031:535–57.

pubmed: 29214591 doi: 10.1007/978-3-319-67144-4_29

Public Health England. Guidance for investigating non-infectious disease clusters from potential environmental causes. London: Public Health England; 2019.

Hoyme HE, Jones KL, Van Allen MI, Saunders BS, Benirschke K. Vascular pathogenesis of transverse limb reduction defects. J Pediatr. 1982;101(5):839–43.

pubmed: 7131173 doi: 10.1016/S0022-3476(82)80343-0

Werler MM, Bosco JL, Shapira SK. Maternal vasoactive exposures, amniotic bands, and terminal transverse limb defects. Birth Defects Res A Clin Mol Teratol. 2009;85(1):52–7.

pubmed: 19067400 pmcid: 2741326 doi: 10.1002/bdra.20524

Bergman JEH, Löhner K, van der Sluis CK, Rump P, de Walle HEK. Etiological diagnosis in limb reduction defects and the number of affected limbs: a population-based study in the Northern Netherlands. Am J Med Genet A. 2020;182(12):2909–18.

pubmed: 32954639 pmcid: 7756893 doi: 10.1002/ajmg.a.61875

McGuirk CK, Westgate MN, Holmes LB. Limb deficiencies in newborn infants. Pediatrics. 2001;108(4):E64.

pubmed: 11581472 doi: 10.1542/peds.108.4.e64

Adrien N, Petersen JM, Parker SE, Werler MM. Vasoactive exposures and risk of amniotic band syndrome and terminal transverse limb deficiencies. Birth Defects Res. 2020;112(14):1074–84.

pubmed: 32573119 pmcid: 9753286 doi: 10.1002/bdr2.1740

Kuldorff M. A spatial scan statistic. Commun Stat Theory Methods. 1997;26:1481–96.

doi: 10.1080/03610929708831995

Gnansia E, Amar E, Harié R, Villessot D, Vargesson N, Aurousseau P, Gillet H. Spatio-temporal aggregate of Transverse Upper Limb Reduction Defects in France (Agrégats spatio-temporels de cas d’agénésie transverse du membre supérieur en France). In French. 2019. Available at: https://www.remera.fr/wp-content/uploads/2019/04/Cluster-ATMS_m%C3%A9thodologie-de-recherche-des-causes-V3-10042019-B.pdf

Cordier S, Garlantézec R, Labat L, Rouget F, Monfort C, Bonvallot N, et al. Exposure during pregnancy to glycol ethers and chlorinated solvents and the risk of congenital malformations. Epidemiology. 2012;23(6):806–12.

pubmed: 23007043 doi: 10.1097/EDE.0b013e31826c2bd8

Garlantézec R, Monfort C, Rouget F, Cordier S. Maternal occupational exposure to solvents and congenital malformations: a prospective study in the general population. Occup Environ Med. 2009;66(7):456–63.

pubmed: 19541806 doi: 10.1136/oem.2008.041772

IRSN (Institut de Radioprotection et de surêté nucléaire). Knowing the radon potential of my commune. Radon file: mapping the radon potential of geological formations. In French and English. Consulted in December 2019 at: https://www.irsn.fr/savoir-comprendre/environnement/connaitre-potentiel-radon-ma-commune

Bentayeb M, Stempfelet M, Wagner V, Zins M, Bonenfant S, Songeur C, Sanchez O, Rosso A, Brulfert G, Rios I, Chaxel E, Virga J, Armengaud A, Rossello P, Rivière E, Bernard M, Vasbien F, Deprost R. Retrospective modeling outdoor air pollution at a fine spatial scale in France, 1989–2008. Atmos Environ. 2014;92:267–79.

doi: 10.1016/j.atmosenv.2014.04.019

Ministère de la santé et de la prévention. SISE-EAUX: Results of the sanitary control of the distributed water commune by commune (Résultats du contrôle sanitaire de l’eau distribuée commune par commune). Consulted in January 2020 at: https://www.data.gouv.fr/en/datasets/resultats-du-controle-sanitaire-de-leau-distribuee-commune-par-commune/

INGF (Institut National de l’Information Géographique et Forestière). Outlines of parcels and crop islands and their main crop group. In French. Consulted in January 2020 at: https://www.data.gouv.fr/fr/datasets/registre-parcellaire-graphique-rpg-contours-des-parcelles-et-ilots-culturaux-et-leur-groupe-de-cultures-majoritaire/

Géorisques, Ministère de la transition écologique et de la cohésion des territoires et BRGM (Etablissement public français pour les applications des sciences de la Terre). CASIAS (Map of Former Industrial Sites and Service Activities) and BASOL (Informing the administration about suspected or actual pollution). In French. Consulted in January 2020 at: https://www.georisques.gouv.fr/donnees/bases-de-donnees/inventaire-historique-de-sites-industriels-et-activites-de-service

GEODERIS, Ministère de la transition écologique et solidaire, BRGM, INERIS. In French. Consulted in February 2020 at: https://geoderis.fr/

Géoservices, INGF. BD TOPO

French Digital Agency (Agence française du numérique). Data visualisation on mobile networks. In French. Consulted in February 2020 at: https://www.data.gouv.fr/fr/organizations/mission-tres-haut-debit/

Barpi, Ministère de la transition écologique et de la cohésion des territoires. ARIA: Feedback on technological accidents. In French and English. Consulted in February 2020 at: https://www.aria.developpement-durable.gouv.fr/?lang=en

Santé publique France. Methodological guide for assessing spatio-temporal aggregates of non-infectious diseases (Guide méthodologique pour l’évaluation des agrégats spatio-temporels de maladies non infectieuses). In French. Saint Maurice: Santé publique France. p. 93. Available at: https://www.santepubliquefrance.fr/docs/guide-methodologique-pour-l-evaluation-des-agregats-spatio-temporelsde-maladies-non-infectieuses

EFSA (European Food Safety Authority) AM, Auteri D, Barmaz S, Bellisai G, Brancato A, Brocca D, Bura L, Byers H, Chiusolo A, Court Marques D, Crivellente F, De Lentdecker C, De Maglie M, Egsmose M, Erdos Z, Fait G, Ferreira L, Goumenou M, Greco L, Ippolito A, Istace F, Jarrah S, Kardassi D, Leuschner R, Lythgo C, Magrans JO, Medina P, Miron I, Molnar T, Nougadere A,Padovani L, Parra Morte JM, Pedersen R, Reich H, Sacchi A, Santos M, Serafimova R, Sharp R, Stanek A,Streissl F, Sturma J, Szentes C, Tarazona J, Terron A, Theobald A, Vagenende B, Verani A, Villamar-Bouza L, 2017. Peer review of the pesticide risk assessment of the active substance bromoxynil (variant evaluated bromoxynil octanoate). EFSA J. 2017;15:24 pages.

Lowry RB, Bedard T. Congenital limb deficiency classification and nomenclature: the need for a consensus. Am J Med Genet A. 2016;170(6):1400–4.

pubmed: 27027980 doi: 10.1002/ajmg.a.37608

Czeizel AE, Elek C, Gundy S, Métneki J, Nemes E, Reis A, et al. Environmental trichlorfon and cluster of congenital abnormalities. Lancet. 1993;341(8844):539–42.

pubmed: 8094783 doi: 10.1016/0140-6736(93)90293-P

Rasmussen SA, Olney RS, Holmes LB, Lin AE, Keppler-Noreuil KM, Moore CA. Guidelines for case classification for the National Birth Defects Prevention Study. Birth Defects Res A Clin Mol Teratol. 2003;67(3):193–201.

pubmed: 12797461 doi: 10.1002/bdra.10012

Khoury MJ, James LM, Flanders WD, Erickson JD. Interpretation of recurring weak associations obtained from epidemiologic studies of suspected human teratogens. Teratology. 1992;46(1):69–77.

pubmed: 1641813 doi: 10.1002/tera.1420460110

Martínez-Frías ML, Bermejo E, Frías JL. Pathogenetic classification of a series of 27,145 consecutive infants with congenital defects. Am J Med Genet. 2000;90(3):246–9.

pubmed: 10678664 doi: 10.1002/(SICI)1096-8628(20000131)90:3<246::AID-AJMG12>3.0.CO;2-Q

Teljeur C, Kelly A, Loane M, Densem J, Dolk H. Using scan statistics for congenital anomalies surveillance: the EUROCAT methodology. Eur J Epidemiol. 2015;30(11):1165–73.

pubmed: 26026722 doi: 10.1007/s10654-015-0044-3

Bellec S, Hémon D, Rudant J, Goubin A, Clavel J. Spatial and space-time clustering of childhood acute leukaemia in France from 1990 to 2000: a nationwide study. Br J Cancer. 2006;94(5):763–70.

pubmed: 16479258 pmcid: 2374236 doi: 10.1038/sj.bjc.6602980

Goujon-Bellec S, Demoury C, Guyot-Goubin A, Hémon D, Clavel J. Detection of clusters of a rare disease over a large territory: performance of cluster detection methods. Int J Health Geogr. 2011;10:53.

pubmed: 21970516 pmcid: 3204219 doi: 10.1186/1476-072X-10-53

Yao Z, Tang J, Zhan FB. Detection of arbitrarily-shaped clusters using a neighbor-expanding approach: a case study on murine typhus in south Texas. Int J Health Geogr. 2011;10:23.

pubmed: 21453514 pmcid: 3079590 doi: 10.1186/1476-072X-10-23

Alexander PG, Clark KL, Tuan RS. Prenatal exposure to environmental factors and congenital limb defects. Birth Defects Res C Embryo Today. 2016;108(3):243–73.

pubmed: 27768243 doi: 10.1002/bdrc.21140

Shirangi A, Nieuwenhuijsen M, Vienneau D, Holman CD. Living near agricultural pesticide applications and the risk of adverse reproductive outcomes: a review of the literature. Paediatr Perinat Epidemiol. 2011;25(2):172–91.

pubmed: 21281330 doi: 10.1111/j.1365-3016.2010.01165.x

Blaisdell J, Turyk ME, Almberg KS, Jones RM, Stayner LT. Prenatal exposure to nitrate in drinking water and the risk of congenital anomalies. Environ Res. 2019;176: 108553.

pubmed: 31325834 pmcid: 6710151 doi: 10.1016/j.envres.2019.108553

Ministère de la santé et de la prévention. Results of health monitoring of tap water quality online, commune by commune in 2011, 2012 and 2013 (Qualité de l’eau potable: résultats du contrôle sanitaire de la qualité de l’eau potable en ligne, commune par commune en 2011,2012 et 2013). In French. Consulted in February 2020 at: https://sante.gouv.fr/sante-et-environnement/eaux/eau

Langlois PH, Lee M, Lupo PJ, Rahbar MH, Cortez RK. Residential radon and birth defects: a population-based assessment. Birth Defects Res A Clin Mol Teratol. 2016;106(1):5–15.

pubmed: 25846606 doi: 10.1002/bdra.23369

Krajewski AK, Rappazzo KM, Langlois PH, Messer LC, Lobdell DT. Associations between cumulative environmental quality and ten selected birth defects in Texas. Birth Defects Res. 2021;113(2):161–72.

pubmed: 32864854 doi: 10.1002/bdr2.1788

Schwartz DA, LoGerfo JP. Congenital limb reduction defects in the agricultural setting. Am J Public Health. 1988;78(6):654–8.

pubmed: 3369595 pmcid: 1350276 doi: 10.2105/AJPH.78.6.654

Ochoa-Acuña H, Carbajo C. Risk of limb birth defects and mother’s home proximity to cornfields. Sci Total Environ. 2009;407(15):4447–51.

pubmed: 19427676 doi: 10.1016/j.scitotenv.2009.04.028

Garry VF, Harkins ME, Erickson LL, Long-Simpson LK, Holland SE, Burroughs BL. Birth defects, season of conception, and sex of children born to pesticide applicators living in the Red River Valley of Minnesota, USA. Environ Health Perspect. 2002;110 Suppl 3(Suppl 3):441–9.

Garry VF, Schreinemachers D, Harkins ME, Griffith J. Pesticide appliers, biocides, and birth defects in rural Minnesota. Environ Health Perspect. 1996;104(4):394–9.

pubmed: 8732949 pmcid: 1469337 doi: 10.1289/ehp.96104394

Lejeune N, Mercier F, Chevrier C, Bonvallot N, Le Bot B. Characterization of multiple pesticide exposure in pregnant women in Brittany, France. J Expo Sci Environ Epidemiol. 2022.

Chaperon L, Oleko A, Pécheux M, Saoudi A, Zeghnoun A.. Impregnation of the French population with amitraz, fipronil, methomyl, bromoxynil and carbendazim (Imprégnation de la population française par l’amitraze, le fipronil, le méthomyl, le bromoxynilet la carbendazime). Programme national de biosurveillance, Esteban 2014–2016. In French. Saint Maurice: Santé publique France; 2022. p. 26.

Yang W, Carmichael SL, Roberts EM, Kegley SE, Padula AM, English PB, et al. Residential agricultural pesticide exposures and risk of neural tube defects and orofacial clefts among offspring in the San Joaquin Valley of California. Am J Epidemiol. 2014;179(6):740–8.

pubmed: 24553680 pmcid: 4271111 doi: 10.1093/aje/kwt324

Zhou Q, Zhang S, Wang Q, Shen H, Zhang Y, Tian W, et al. Association between preconception paternal smoking and birth defects in offspring: evidence from the database of the National Free Preconception Health Examination Project in China. BJOG. 2020;127(11):1358–64.

pubmed: 32339375 doi: 10.1111/1471-0528.16277

Källén K. Maternal smoking during pregnancy and limb reduction malformations in Sweden. Am J Public Health. 1997;87(1):29–32.

pubmed: 9065222 pmcid: 1380760 doi: 10.2105/AJPH.87.1.29

Caspers KM, Romitti PA, Lin S, Olney RS, Holmes LB, Werler MM. Maternal periconceptional exposure to cigarette smoking and congenital limb deficiencies. Paediatr Perinat Epidemiol. 2013;27(6):509–20.

pubmed: 24134526 pmcid: 4445653 doi: 10.1111/ppe.12075

Hackshaw A, Rodeck C, Boniface S. Maternal smoking in pregnancy and birth defects: a systematic review based on 173 687 malformed cases and 11.7 million controls. Hum Reprod Update. 2011;17(5):589–604.

pubmed: 21747128 pmcid: 3156888 doi: 10.1093/humupd/dmr022

Leite M, Albieri V, Kjaer SK, Jensen A. Maternal smoking in pregnancy and risk for congenital malformations: results of a Danish register-based cohort study. Acta Obstet Gynecol Scand. 2014;93(8):825–34.

pubmed: 24861914 doi: 10.1111/aogs.12433

Klungsøyr K, Nordtveit TI, Kaastad TS, Solberg S, Sletten IN, Vik AK. Epidemiology of limb reduction defects as registered in the Medical Birth Registry of Norway, 1970–2016: population based study. PLoS ONE. 2019;14(7): e0219930.

pubmed: 31314783 pmcid: 6636750 doi: 10.1371/journal.pone.0219930

Syvänen J, Nietosvaara Y, Hurme S, Perheentupa A, Gissler M, Raitio A, et al. Maternal risk factors for congenital limb deficiencies: a population-based case-control study. Paediatr Perinat Epidemiol. 2021;35(4):450–8.

pubmed: 33438777 doi: 10.1111/ppe.12740

Materna-Kiryluk A, Wisniewska K, Wieckowska B, Wierzba J, Jazdzewska A, Jaroszewska-Swiatek B, et al. Maternal risk factors associated with limb reduction defects: data from the Polish Registry of Congenital Malformations (PRCM). Children (Basel). 2021;8(2):138.

pubmed: 33673226 pmcid: 7918052

Robitaille J, Carmichael SL, Shaw GM, Olney RS. Maternal nutrient intake and risks for transverse and longitudinal limb deficiencies: data from the National Birth Defects Prevention Study, 1997–2003. Birth Defects Res A Clin Mol Teratol. 2009;85(9):773–9.

pubmed: 19350655 doi: 10.1002/bdra.20587

Hunter AG. A pilot study of the possible role of familial defects in anticoagulation as a cause for terminal limb reduction malformations. Clin Genet. 2000;57(3):197–204.

pubmed: 10782926 doi: 10.1034/j.1399-0004.2000.570305.x

Ordal L, Keunen J, Martin N, Shehata N, Borschel GH, Clarke HM, et al. Congenital limb deficiencies with vascular etiology: possible association with maternal thrombophilia. Am J Med Genet A. 2016;170(12):3083–9.

pubmed: 27530094 doi: 10.1002/ajmg.a.37890

Rockenbauer M, Olsen J, Czeizel AE, Pedersen L, Sørensen HT. Recall bias in a case-control surveillance system on the use of medicine during pregnancy. Epidemiology. 2001;12(4):461–6.

pubmed: 11416783 doi: 10.1097/00001648-200107000-00017

Ministère de la Santé et de la Prévention. Roadmap for the surveillance and understanding of risk factors for congenital malformations, including Transverse Upper Limb Reduction Defects (Feuille de route pour la surveillance et la connaissance des facteurs de risque des malformations congénitales incluant les ATMS). In French. 2020. Available at: https://sante.gouv.fr/IMG/pdf/feuille_de_route.pdf

Tuppin P, Rudant J, Constantinou P, Gastaldi-Ménager C, Rachas A, de Roquefeuil L, et al. Value of a national administrative database to guide public decisions: From the système national d’information interrégimes de l’Assurance Maladie (SNIIRAM) to the système national des données de santé (SNDS) in France. Rev Epidemiol Sante Publique. 2017;65(Suppl 4):S149–67.

pubmed: 28756037 doi: 10.1016/j.respe.2017.05.004