The cost-effectiveness of neonatal versus prenatal screening for congenital toxoplasmosis


Autoři: Christine Binquet aff001;  Catherine Lejeune aff001;  Valérie Seror aff003;  François Peyron aff005;  Anne-Claire Bertaux aff001;  Olivier Scemama aff007;  Catherine Quantin aff001;  Sophie Béjean aff010;  Eileen Stillwaggon aff012;  Martine Wallon aff005
Působiště autorů: INSERM, CIC1432, Module Epidémiologie Clinique, Dijon, France aff001;  Centre Hospitalier Universitaire Dijon-Bourgogne, Centre d’investigation Clinique, Module Épidémiologie Clinique/ Essais Cliniques, Dijon, France aff002;  Aix Marseille Univ, IRD, AP-HM, SSA, VITROME, Marseille, France aff003;  IHU-Méditerranée Infection, Marseille, France aff004;  Hospices Civils de Lyon, Hôpital de la Croix-Rousse, Institut de Parasitologie et de Mycologie Médicale, Institut des Agents Infectieux, Lyon, France aff005;  Centre Hospitalier Universitaire Dijon-Bourgogne, Délégation à la recherche Clinique et à l’Innovation, Unité de Soutien Méthodologique à la Recherche, Dijon, France aff006;  Haute Autorité de Santé, Service Evaluation Economique et Santé Publique, St Denis, France aff007;  Centre Hospitalier Universitaire Dijon-Bourgogne, Service de biostatistiques et d’informatique médicale, Dijon, France aff008;  INSERM, UVSQ, Institut Pasteur, Université Paris-Saclay, Biostatistics, Biomathematics, Pharmacoepidemiology and Infectious Diseases (B2PHI), Paris, France aff009;  Université de Bourgogne, Laboratoire d’économie de Dijon, Dijon, France aff010;  CNRS, UMR 6307, Dijon, France aff011;  Department of Economics, Gettysburg College, Gettysburg, Pennsylvania, United states of America aff012;  INSERM, U1028, Physiologie Intégrée du Système d’Eveil, Lyon, France aff013;  CNRS, UMR5292, Lyon, France aff014;  Université Lyon, Centre de Recherche en Neurosciences, Lyon, France aff015
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0221709

Souhrn

Background

Congenital Toxoplasmosis (CT) can have severe consequences. France, Austria, and Slovenia have prenatal screening programs whereas some other countries are considering universal screening to reduce congenital transmission and severity of infection in children. The efficiency of such programs is debated increasingly as seroprevalence among pregnant women and incidence of congenital toxoplasmosis show a steady decrease. In addition, uncertainty remains regarding the effectiveness of pre- and postnatal treatments.

Method

To identify cost-effective strategies, prenatal and neonatal screenings were compared using a decision-analytic model based on French guidelines and current knowledge of long-term evolution of the disease in treated children. Epidemiological data were extracted from the scientific literature and clinical data from the French Lyon cohort. Strategies were compared at one year of age, when infection can be definitively evaluated, and at 15 years of age, after which validated outcome data become scarce. The analysis was performed from the French Health Insurance System perspective and included direct medical costs for pregnant women and their children.

Results

The 1-year Incremental Cost-Effectiveness Ratio showed that prenatal screening would require investing €14,826 to avoid one adverse event (liveborn with CT, fetal loss, neonatal death or pregnancy termination) compared to neonatal screening. Extra investment increased up to €21,472 when considering the 15-year endpoint.

Conclusions

Prenatal screening is cost-effective as compared to neonatal screening in moderate prevalence areas with predominant Type II strains. In addition, prenatal screening, by providing closer follow-up of women at risk increases the number of occasions for education avoiding toxoplasmosis.

Klíčová slova:

Medicine and health sciences – Parasitic diseases – Protozoan infections – Toxoplasmosis – Women's health – Maternal health – Pregnancy – Pregnancy complications – Fetal death – Birth – Obstetrics and gynecology – Pediatrics – Pediatric infections – Biology and life sciences – Developmental biology – Neonates – Engineering and technology – Management engineering – Research and analysis methods – Decision analysis – Decision trees – Social sciences – Economics – Economic analysis – Cost-effectiveness analysis


Zdroje

1. Dubey JP, Jones JL (2008) Toxoplasma gondii infection in humans and animals in the United States. Int J Parasitol 38: 1257–1278. doi: 10.1016/j.ijpara.2008.03.007 18508057

2. Tenter AM, Heckeroth AR, Weiss LM (2000) Toxoplasma gondii: from animals to humans. Int J Parasitol 30: 1217–1258. doi: 10.1016/s0020-7519(00)00124-7 11113252

3. Phan L, Kasza K, Jalbrzikowski J, Noble AG, Latkany P, Kuo A, et al. (2008) Longitudinal study of new eye lesions in children with toxoplasmosis who were not treated during the first year of life. Am J Ophthalmol 146: 375–384. doi: 10.1016/j.ajo.2008.04.033 18619570

4. McLeod R, Boyer KM, Lee D, Mui E, Wroblewski K, Karisson T, et al. (2012) Prematurity and severity are associated with Toxoplasma gondii alleles (NCCCTS, 1981–2009). Clin Infect Dis 54: 1595–1605. doi: 10.1093/cid/cis258 22499837

5. Wallon M, Peyron F, Cornu C, Vinault S, Abrahamowicz M, Bonithon-Kopp C, et al. (2013) Congenital toxoplasma infection: monthly prenatal screening decreases transmission rate and improves clinical outcome at age 3 years. Clin Infect Dis 56: 1223–1231. doi: 10.1093/cid/cit032 23362291

6. Wallon M, Garweg JG, Abrahamowicz M, Cornu C, Vinault S, Quantin C, et al. (2014) Ophthalmic outcomes of congenital toxoplasmosis followed until adolescence. Pediatrics 133: e601–608. doi: 10.1542/peds.2013-2153 24534412

7. Syrocot Study group, Thiebaut R, Leproust S, Chene G, Gilbert R (2007) Effectiveness of prenatal treatment for congenital toxoplasmosis: a meta-analysis of individual patients’ data. Lancet 369: 115–122. doi: 10.1016/S0140-6736(07)60072-5 17223474

8. Prusa AR, Kasper DC, Pollak A, Gleiss A, Waldhoer T, Hayde M. (2015) The Austrian Toxoplasmosis Register, 1992–2008. Clin Infect Dis 60: e4–e10. doi: 10.1093/cid/ciu724 25216688

9. Roser D, Nielsen HV, Petersen E, Saugmann-Jensen P, Norgaard-Pedersen B (2010) Congenital toxoplasmosis—a report on the Danish neonatal screening programme 1999–2007. J Inherit Metab Dis 33: S241–247.

10. Gomez-Marin JE, Montoya-de-Londono MT, Castano-Osorio JC (1997) A maternal screening program for congenital toxoplasmosis in Quindio, Colombia and application of mathematical models to estimate incidences using age-stratified data. Am J Trop Med Hyg 57: 180–186. doi: 10.4269/ajtmh.1997.57.180 9288813

11. Tan-Torres Edejer T, Baltussen R, Adam T, Hutubessy R, Acharya A, Evans DB, et al. (2003) Making choices in health: WHO guide to cost-effectiveness analysis. Geneva: WHO.

12. Haute Autorité de Santé (2011) Choix méthodologiques pour l'évaluation économique à la HAS. Paris, France: Haute Autorité de Santé. 83 p.

13. Peyron F, L’Ollivier C, Mandelbrot L, Wallon M, Piarroux R, Kieffer F, et al. (2019) Maternal and Congenital Toxoplasmosis: Diagnosis and Treatment Recommendations of a French Multidisciplinary Working Group. Pathogens 8.

14. Pappas G, Roussos N, Falagas ME (2009) Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int J Parasitol 39: 1385–1394. doi: 10.1016/j.ijpara.2009.04.003 19433092

15. Tourdjman M, Tchéandjieu C, de Valk H, Goulet V, Le Strat Y (2015) Toxoplasmose chez les femmes enceintes en France: évolution de la séroprévalence et des facteurs associés entre 1995 et 2010, à partir des Enquêtes nationales périnatales. Bull Epidemio Hebd: 264–272.

16. Jones JL, Kruszon-Moran D, Sanders-Lewis K, Wilson M (2007) Toxoplasma gondii infection in the United States, 1999 2004, decline from the prior decade. Am J Trop Med Hyg 77: 405–410. 17827351

17. Petersson K, Stray-Pedersen B, Malm G, Forsgren M, Evengard B (2000) Seroprevalence of Toxoplasma gondii among pregnant women in Sweden. Acta Obstet Gynecol Scand 79: 824–829. 11304963

18. Nogareda F, Le Strat Y, Villena I, De Valk H, Goulet V (2014) Incidence and prevalence of Toxoplasma gondii infection in women in France, 1980–2020: model-based estimation. Epidemiol Infect 142: 1661–1670. doi: 10.1017/S0950268813002756 24229712

19. Evengard B, Petersson K, Engman ML, Wiklund S, Ivarsson SA, Tear-Fahnehjelm K, et al. (2001) Low incidence of toxoplasma infection during pregnancy and in newborns in Sweden. Epidemiol Infect 127: 121–127. doi: 10.1017/s0950268801005775 11561964

20. Torgerson PR, Mastroiacovo P (2013) The global burden of congenital toxoplasmosis: a systematic review. Bull World Health Organ 91: 501–508. doi: 10.2471/BLT.12.111732 23825877

21. Robert-Gangneux F, Darde ML (2012) Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev 25: 264–296. doi: 10.1128/CMR.05013-11 22491772

22. Jenum PA, Stray-Pedersen B, Melby KK, Kapperud G, Whitelaw A, Eskild A, et al. (1998) Incidence of Toxoplasma gondii infection in 35,940 pregnant women in Norway and pregnancy outcome for infected women. J Clin Microbiol 36: 2900–2906. 9738041

23. Carrera JM, Torrents M, Mortera C, Cusi V, Munoz A (1995) Routine prenatal ultrasound screening for fetal abnormalities: 22 years’ experience. Ultrasound Obstet Gynecol 5: 174–179. doi: 10.1046/j.1469-0705.1995.05030174.x 7788491

24. Chitty LS, Hunt GH, Moore J, Lobb MO (1991) Effectiveness of routine ultrasonography in detecting fetal structural abnormalities in a low risk population. BMJ 303: 1165–1169. doi: 10.1136/bmj.303.6811.1165 1747613

25. Ewigman B, LeFevre M, Hesser J (1990) A randomized trial of routine prenatal ultrasound. Obstet Gynecol 76: 189–194. 2196496

26. Grandjean H, Larroque D, Levi S (1999) The performance of routine ultrasonographic screening of pregnancies in the Eurofetus Study. Am J Obstet Gynecol 181: 446–454. doi: 10.1016/s0002-9378(99)70577-6 10454699

27. Levi S (2002) Ultrasound in prenatal diagnosis: polemics around routine ultrasound screening for second trimester fetal malformations. Prenat Diagn 22: 285–295. doi: 10.1002/pd.306 11981909

28. Morris JK, Springett AL, Greenlees R, Loane M, Addor MC, Arriola L, et al. (2018) Trends in congenital anomalies in Europe from 1980 to 2012. PLoS One 13: e0194986. doi: 10.1371/journal.pone.0194986 29621304

29. Nybo Andersen AM, Wohlfahrt J, Christens P, Olsen J, Melbye M (2000) Maternal age and fetal loss: population based register linkage study. BMJ 320: 1708–1712. doi: 10.1136/bmj.320.7251.1708 10864550

30. Delabaere A, Huchon C, Deffieux X, Beucher G, Gallot V, Nedellec S, et al. (2014) [Epidemiology of loss pregnancy]. J Gynecol Obstet Biol Reprod (Paris) 43: 764–775.

31. Pilkington H, Blondel B, Drewniak N, Zeitlin J (2014) Where does distance matter? Distance to the closest maternity unit and risk of foetal and neonatal mortality in France. Eur J Public Health 24: 905–910. doi: 10.1093/eurpub/ckt207 24390464

32. Montoya JG, Remington JS (2008) Management of Toxoplasma gondii infection during pregnancy. Clin Infect Dis 47: 554–566. doi: 10.1086/590149 18624630

33. Dunn D, Wallon M, Peyron F, Petersen E, Peckham C, Gilbert R, et al. (1999) Mother-to-child transmission of toxoplasmosis: risk estimates for clinical counselling. Lancet 353: 1829–1833. doi: 10.1016/S0140-6736(98)08220-8 10359407

34. Haute Autorité de Santé (2009) Surveillance sérologique et prévention de la toxoplasmose et de la rubéole au cours de la grossesse et dépistage prénatal de l’hépatite B–Pertinence des modalités de réalisation. Paris, France: Haute Autorité de Santé.

35. Ewigman BG, Crane JP, Frigoletto FD, Le Fevre ML, Bain RP, McNellis D. (1993) Effect of prenatal ultrasound screening on perinatal outcome. RADIUS Study Group. N Engl J Med 329: 821–827. doi: 10.1056/NEJM199309163291201 8355740

36. Brocks V, Bang J (1991) Routine examination by ultrasound for the detection of fetal malformations in a low risk population. Fetal Diagn Ther 6: 37–45. doi: 10.1159/000263623 1768345

37. Goncalves LF, Jeanty P, Piper JM (1994) The accuracy of prenatal ultrasonography in detecting congenital anomalies. Am J Obstet Gynecol 171: 1606–1612. doi: 10.1016/0002-9378(94)90411-1 7802077

38. Wallon M, Franck J, Thulliez P, Huissoud C, Peyron F, Garcia-Merci P, et al. (2010) Accuracy of real-time polymerase chain reaction for Toxoplasma gondii in amniotic fluid. Obstet Gynecol 115: 727–733. doi: 10.1097/AOG.0b013e3181d57b09 20308831

39. de Oliveira Azevedo CT, do Brasil PE, Guida L, Lopes Moreira ME (2016) Performance of Polymerase Chain Reaction Analysis of the Amniotic Fluid of Pregnant Women for Diagnosis of Congenital Toxoplasmosis: A Systematic Review and Meta-Analysis. PLoS One 11: e0149938. doi: 10.1371/journal.pone.0149938 27055272

40. Lebech M, Andersen O, Christensen NC, Hertel J, Nielsen HE, et al. (1999) Feasibility of neonatal screening for toxoplasma infection in the absence of prenatal treatment. Danish Congenital Toxoplasmosis Study Group. Lancet 353: 1834–1837. doi: 10.1016/s0140-6736(98)11281-3 10359408

41. Naessens A, Jenum PA, Pollak A, Decoster A, Lappalainen M, Villena I, et al. (1999) Diagnosis of congenital toxoplasmosis in the neonatal period: A multicenter evaluation. J Pediatr 135: 714–719. doi: 10.1016/s0022-3476(99)70090-9 10586174

42. Naot Y, Desmonts G, Remington JS (1981) IgM enzyme-linked immunosorbent assay test for the diagnosis of congenital Toxoplasma infection. J Pediatr 98: 32–36. doi: 10.1016/s0022-3476(81)80528-8 7452400

43. Robert-Gangneux F, Gavinet MF, Ancelle T, Raymond J, Tourte-Schaefer C, Dupouy-CAmet J. (1999) Value of prenatal diagnosis and early postnatal diagnosis of congenital toxoplasmosis: retrospective study of 110 cases. J Clin Microbiol 37: 2893–2898. 10449471

44. Rodrigues IM, Castro AM, Gomes MB, Amaral WN, Avelino MM (2009) Congenital toxoplasmosis: evaluation of serological methods for the detection of anti-Toxoplasma gondii IgM and IgA antibodies. Mem Inst Oswaldo Cruz 104: 434–440. doi: 10.1590/s0074-02762009000300006 19547868

45. Paul M (2007) Serological Screening of Newborns for Toxoplasma Gondii-Specific IgA and IgM Antibodies in Peripheral Blood Collected on Filter-Papers. EJIFCC 18: 91–114. 29606933

46. Cornu C, Bissery A, Malbos C, Garwig R, Cocherel C, Ecochard R, et al. (2009) Factors affecting the adherence to an antenatal screening programme: an experience with toxoplasmosis screening in France. Euro Surveill 14: 21–25. 19317970

47. Wallon M, Liou C, Garner P, Peyron F (1999) Congenital toxoplasmosis: systematic review of evidence of efficacy of treatment in pregnancy. BMJ 318: 1511–1514. doi: 10.1136/bmj.318.7197.1511 10356003

48. Chene G, Thiebaut R (2009) Options for clinical trials of pre and post-natal treatments for congenital toxoplasmosis. Mem Inst Oswaldo Cruz 104: 299–304. doi: 10.1590/s0074-02762009000200025 19430657

49. Holliman RE (1995) Congenital toxoplasmosis: prevention, screening and treatment. J Hosp Infect 30 Suppl: 179–190.

50. Derouin F, Gerard L, Farinotti R, Maslo C, Leport C (1998) Determination of the inhibitory effect on Toxoplasma growth in the serum of AIDS patients during acute therapy for toxoplasmic encephalitis. J Acquir Immune Defic Syndr Hum Retrovirol 19: 50–54. 9732069

51. Derouin F, Nalpas J, Chastang C (1988) [In vitro measurement of the inhibitory effect of macrolides, lincosamides and synergestines on the growth of Toxoplasma gondii]. Pathol Biol (Paris) 36: 1204–1210.

52. Foulon W, Villena I, Stray-Pedersen B, Decoster A, Lappalainen M, Pinon JM, et al. (1999) Treatment of toxoplasmosis during pregnancy: a multicenter study of impact on fetal transmission and children’s sequelae at age 1 year. Am J Obstet Gynecol 180: 410–415. doi: 10.1016/s0002-9378(99)70224-3 9988811

53. Marseille E, Larson B, Kazi DS, Kahn JG, Rosen S (2015) Thresholds for the cost-effectiveness of interventions: alternative approaches. Bull World Health Organ 93: 118–124. doi: 10.2471/BLT.14.138206 25883405

54. Stillwaggon E, Carrier CS, Sautter M, McLeod R (2011) Maternal serologic screening to prevent congenital toxoplasmosis: a decision-analytic economic model. PLoS Negl Trop Dis 5: e1333. doi: 10.1371/journal.pntd.0001333 21980546

55. Prusa AR, Kasper DC, Sawers L, Walter E, Hayde M, Stilwaggon E. (2017) Congenital toxoplasmosis in Austria: Prenatal screening for prevention is cost-saving. PLoS Negl Trop Dis 11: e0005648. doi: 10.1371/journal.pntd.0005648 28692640

56. El Bissati K, Levigne P, Lykins J, Adlaoui EB, Barkat A, Berraho A, et al. (2018) Global initiative for congenital toxoplasmosis: an observational and international comparative clinical analysis. Emerg Microbes Infect 7: 165. doi: 10.1038/s41426-018-0164-4 30262847

57. Girard D, Leclercq A, Laurent E, Lecuit M, de Valk H, Goulet V. (2014) Pregnancy-related listeriosis in France, 1984 to 2011, with a focus on 606 cases from 1999 to 2011. Euro Surveill 19.

58. Brown AS, Schaefer CA, Quesenberry CP Jr., Liu L, Babulas VP, Susser ES. (2005) Maternal exposure to toxoplasmosis and risk of schizophrenia in adult offspring. Am J Psychiatry 162: 767–773. doi: 10.1176/appi.ajp.162.4.767 15800151

59. Bianchi CM, Huneau JF, Le Goff G, Verger EO, Mariotti F, Gurviez P. (2016) Concerns, attitudes, beliefs and information seeking practices with respect to nutrition-related issues: a qualitative study in French pregnant women. BMC Pregnancy Childbirth 16: 306. doi: 10.1186/s12884-016-1078-6 27729021

60. Begeman IJ, Lykins J, Zhou Y, Lai BS, Levigne P, El Bissati K, et al. (2017) Point-of-care testing for Toxoplasma gondii IgG/IgM using Toxoplasma ICT IgG-IgM test with sera from the United States and implications for developing countries. PLoS Negl Trop Dis 11: e0005670. doi: 10.1371/journal.pntd.0005670 28650970

61. Lykins J, Li X, Levigne P, Zhou Y, El Bissati K, Clouser F, et al. (2018) Rapid, inexpensive, fingerstick, whole-blood, sensitive, specific, point-of-care test for anti-Toxoplasma antibodies. PLoS Negl Trop Dis 12: e0006536. doi: 10.1371/journal.pntd.0006536 30114251

62. Chapey E, Meroni V, Kieffer F, Bollani L, Ecochard R, Garcia P, et al. (2015) Use of IgG in oral fluid to monitor infants with suspected congenital toxoplasmosis. Clin Vaccine Immunol 22: 398–403. doi: 10.1128/CVI.00552-14 25651923


Článek vyšel v časopise

PLOS One


2019 Číslo 9

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Ulcerative colitis_muž_břicho_střeva
Ulcerózní kolitida
nový kurz
Autoři:

Blokátory angiotenzinových receptorů (sartany)
Autoři: MUDr. Jiří Krupička, Ph.D.

Antiseptika a prevence ve stomatologii
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Citikolin v neuroprotekci a neuroregeneraci: od výzkumu do klinické praxe nejen očních lékařů
Autoři: MUDr. Petr Výborný, CSc., FEBO

Zánětlivá bolest zad a axiální spondylartritida – Diagnostika a referenční strategie
Autoři: MUDr. Monika Gregová, Ph.D., MUDr. Kristýna Bubová

Všechny kurzy