Objective To determine a cost-minimizing option for congenital toxoplasmosis in the United States. Methodology/Principal Findings A decision-analytic and cost-minimization model was constructed to compare monthly maternal serological screening, prenatal treatment, and post-natal follow-up and treatment according to the current French (Paris) protocol, versus no systematic screening or perinatal treatment. Costs are based on published estimates of lifetime societal costs of developmental disabilities and current diagnostic and treatment costs. Probabilities are based on published results and clinical practice in the United States and France. One- and two-way sensitivity analyses are used to evaluate robustness of results. Universal monthly maternal screening for congenital toxoplasmosis with follow-up and treatment, following the French protocol, is found to be cost-saving, with savings of $620 per child screened. Results are robust to changes in test costs, value of statistical life, seroprevalence in women of childbearing age, fetal loss due to amniocentesis, and to bivariate analysis of test costs and incidence of primary T. gondii infection in pregnancy. Given the parameters in this model and a maternal screening test cost of $12, screening is cost-saving for rates of congenital infection above 1 per 10,000 live births. If universal testing generates economies of scale in diagnostic tools—lowering test costs to about $2 per test—universal screening is cost-saving at rates of congenital infection well below the lowest reported rates in the United States of 1 per 10,000 live births. Conclusion/Significance Universal screening according to the French protocol is cost saving for the US population within broad parameters for costs and probabilities.
References
[1]
Eichenwald HF (1960) A study of congenital toxoplasmosis, with particular emphasis on clinical manifestations, sequelae and therapy. In: Siim JC, editor. Human toxoplasmosis. Munksgaard, Copenhagen. pp. 41–49.
[2]
Wilson CB, Remington JS, Stagno S, Reynolds DW (1980) Development of adverse sequelae in children born with subclinical congenital Toxoplasma infection. Pediatrics 66: 767–774.
[3]
Koppe JG, Loewer-Sieger DH, de Roever-Bonnet H (1986) Results of 20-year follow-up of congenital toxoplasmosis. Lancet 327: 254–256. doi: 10.1016/S0140-6736(86)90785-3
McAuley J, Boyer KM, Patel D, Mets M, Swisher C, et al. (1994) Early and longitudinal evaluations of treated infants and children and untreated historical patients with congenital toxoplasmosis: The Chicago collaborative treatment trial. Clinical Infectious Diseases 18: 38–72. doi: 10.1093/clinids/18.1.38
[6]
McLeod R, Boyer K, Karrison T, Kasza K, Swisher C, et al. (2006) Outcome of treatment for congenital toxoplasmosis, 1981-2004: The national collaborative Chicago-based, congenital toxoplasmosis study. Clinical Infectious Diseases 42: 1383–1394. doi: 10.1086/501360
[7]
Phan L, Kasza K, Jalbrzikowski J, Noble AG, Latkany P, et al. (2008) Longitudinal study of new eye lesions in treated congenital toxoplasmosis. Ophthalmology 115: 553–559. doi: 10.1016/j.ophtha.2007.06.022
[8]
Phan L, Kasza K, Jalbrzikowski J, Noble AG, Latkany P, et al. (2008) Longitudinal study of new eye lesions in children with toxoplasmosis who were not treated during the first year of life. American Journal of Ophthalmology 146: 375–384. doi: 10.1016/j.ajo.2008.04.033
[9]
McLeod R, Kieffer F, Sautter M, Hosten T, Pelloux H (2009) Why prevent, diagnose and treat congenital toxoplasmosis? . Memorias do Instituto Oswaldo Cruz 104: 320–344. doi: 10.1590/S0074-02762009000200029
[10]
Swisher CN, Boyer K, McLeod R (1994) The Toxoplasmosis Study Group. Congenital toxoplasmosis. Semin Pediatr Neurol 1: 4–25.
[11]
Mets MB, Holfels E, Boyer KM, Swisher CN, Roizen N, et al. (1996) Eye manifestations of congenital toxoplasmosis. American Journal of Ophthalmology 122: 309–324.
[12]
McLeod R, Mack D, Foss R, Boyer K, Withers S, et al. (1992) Levels of pyrimethamine in sera and cerebrospinal and ventricular fluids from infants treated for congenital toxoplasmosis. Antimicrobial agents and chemotherapy 36: 1040–1048. doi: 10.1128/AAC.36.5.1040
[13]
Couvreur J, Desmonts G (1962) Congenital and maternal toxoplasmosis. A review of 300 congenital cases. Developmental Medicine and Child Neurology 4: 519–530. doi: 10.1111/j.1469-8749.1962.tb03221.x
[14]
Thulliez P (2001) Commentary: Efficacy of prenatal treatment for toxoplasmosis: a possibility that cannot be ruled out. Int J Epidemiol 30: 1315–1316. doi: 10.1093/ije/30.6.1315
[15]
Hohlfeld P, Daffos F, Thulliez P, Aufrant C, Couvreur J, et al. (1989) Fetal toxoplasmosis: Outcome of pregnancy and infant follow-up after in utero treatment. Journal of Pediatrics 115: 765–769. doi: 10.1016/S0022-3476(89)80660-2
[16]
Brézin AP, Thulliez P, Couvreur J, Nobré R, Mcleod R, et al. (2003) Ophthalmic outcomes after prenatal and postnatal treatment of congenital toxoplasmosis. American Journal of Ophthalmology 135: 779–784. doi: 10.1016/S0002-9394(02)01704-X
[17]
Kieffer F, Wallon M, Garcia P, Thulliez P, Peyron F, et al. (2008) Risk factors for retinochoroiditis during the first 2 years of life in infants with treated congenital toxoplasmosis. Pediatr Infect Dis J 27: 27–32. doi: 10.1097/INF.0b013e318134286d
[18]
Wallon M, Kodjikian L, Binquet C, Garweg J, Fleury J, et al. (2004) Long-term ocular prognosis in 327 children with congenital toxoplasmosis. Pediatrics 113: 1567–1572. doi: 10.1542/peds.113.6.1567
[19]
Thiébaut R, Leproust S, Chêne G, Gilbert R, SYROCOT - Systematic Review on Congenital Toxoplasmosis Study Group (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
[20]
Peyron F, Garweg JG, Wallon M, Descloux E, Rolland M, et al. (2011) Long-term Impact of Treated Congenital Toxoplasmosis on Quality of Life and Visual Performance. Pediatr Infect Dis J 30: 597–600. doi: 10.1097/INF.0b013e31820bb5f3
[21]
Cortina-Borja M, Tan HK, Wallon M, Paul M, Prusa A, et al. (2010) Prenatal Treatment for Serious Neurological Sequelae of Congenital Toxoplasmosis: An Observational Prospective Cohort Study. PLOS Medicine 7: 1–11. doi: 10.1371/journal.pmed.1000351
[22]
Foulon W, Villena I, Stray-Pedersen B, Decoster A, Lappalainen M, et al. (1999) Treatment of toxoplasmosis during pregnancy: A multicenter study of impact on fetal transmission and children's sequelae at age 1 year. American Journal of Obstetrics and Gynecology 180: 410–415. doi: 10.1016/S0002-9378(99)70224-3
[23]
Vasconcelos-Santos DV, Machado Azevedo DO, Campos WR, Oréfice F, Queiroz-Andrade GM, et al. (2009) Congenital toxoplasmosis in southeastern Brazil: results of early ophthalmologic examination of a large cohort of neonates. Ophthalmology 116: 2199–2205. doi: 10.1016/j.ophtha.2009.04.042
[24]
Mui EJ, Schiehser GA, Milhous WK, Hsu H, Roberts CW, et al. (2008) Novel triazine JPC-2067-B inhibits Toxoplasma gondii in vitro and in vivo. PLoS Negl Trop Dis 2: e190. doi: 10.1371/journal.pntd.0000190
[25]
Jones JL, Kruszon-Moran D, Wilson M, McQuillan G, Navin T, et al. (2001) Toxoplasma gondii Infection in the United States: Seroprevalence and Risk Factors. American Journal of Epidemiology 154: 357–365. doi: 10.1093/aje/154.4.357
[26]
Jones JL, Kruszon-Moran D, Wilson M (2003) Toxoplasma gondii infection in the United States, 1999-2000. Emerging Infectious Diseases 9: 1371–1374. doi: 10.3201/eid0911.030098
[27]
Gilbert RE, Freeman K, Lago EG, Bahia-Oliveira LM, Tan HK, et al. (2008) Ocular sequelae of congenital toxoplasmosis in Brazil compared with Europe. PLoS Negl Trop Dis 2: e277. doi: 10.1371/journal.pntd.0000277
[28]
Hill D, Boyer K, Mui E, Kasza K, Karrison T, et al. (2011) Unrecognized ingestion of Toxoplasma oocysts causes congenital toxoplasmosis and epidemics in North America. Clin Infect Dis, in press. doi: 10.1016/j.ynpm.2011.12.013
[29]
Hill D, Coss C, Dubey JP, Wroblewski K, Sautter M, et al. (2011) Identification of a sporozoite-specific antigen from Toxoplasma gondii. J Parasitol 97: 328–337. doi: 10.1645/GE-2782.1
[30]
Darde ML (2004) Genetic analysis of the diversity in Toxoplasma gondii. Ann Inst Super Sanita 40: 57–63.
[31]
Howe DK, Hono？e S, Derouin F, Sibley LD (1997) Determination of genotypes of Toxoplasma gondii strains isolated from patients with toxoplasmosis. J Clin Microbiol 35: 1411–1414.
[32]
Grigg ME, Ganatra J, Boothroyd JC, Margolis TP (2001) Unusual abundance of atypical strains associated with human ocular toxoplasmosis. J Infect Dis 84: 633–639. doi: 10.1086/322800
[33]
Lehmann T, Marcet PL, Graham DH, Dahl ER, Dubey JP (2006) Globalization and the population structure of Toxoplasma gondii. Proc Natl Acad Sci USA 103: 11423–11428. doi: 10.1073/pnas.0601438103
[34]
Khan A, Jordan C, Muccioli C, Vallochi AL, Rizzo LV, et al. (2006) Genetic divergence of Toxoplasma gondii strains associated with ocular toxoplasmosis, Brazil. Emerg Infect Dis 12: 942–949. doi: 10.3201/eid1206.060025
[35]
Gomez-Marin JE, de la Torre A (2007) Positive benefit of postnatal treatment in congenital toxoplasmosis. Arch Dis Child 92: 88–89.
[36]
de la Torre A, Gonzalez G, Diaz-Ramirez J, Gomez-Marin JE (2007) Screening by ophthalmoscopy for Toxoplasma retinochoroiditis in Colombia. Am J Ophthalmol 143: 354–356. doi: 10.1016/j.ajo.2006.09.048
[37]
Gallego C, Saavedra-Matiz C, Gomez-Marin JE (2006) Direct genotyping of animal and human isolates of Toxoplasma gondii from Colombia (South America). Acta Trop 97: 161–167. doi: 10.1016/j.actatropica.2005.10.001
[38]
Dubey JP, Velmurugan G, Rajendran C, Yabsley Y, Thomas N, et al. (2011) Genetic？ characterisation ？of ？Toxoplasma？ gondii ？in？ wild life ？from ？North？ America？revealed？widespread？and？high？pre？valence？of？the？fourth？clonal？type. International？Journal？for？Parasitology, in press. available on line 19 July 2011.
[39]
Dubey JP, Rajendran C, Ferreira LR, Martins J, Kwok OCH, et al. (2011) High prevalence and genotypes of Toxoplasma gondii isolated from goats, from a retail meat store, destined for human consumption in the USA. International Journal for Parasitology 41: 827–833. doi: 10.1016/j.ijpara.2011.03.006
[40]
Khan A, Dubey JP, Su C, Ajioka JW, Rosenthal BM, et al. (2011) Genetic analyses of atypical Toxoplasma gondii strains reveal a fourth clonal lineage in North America. International Journal for Parasitology 41: 645–655. doi: 10.1016/j.ijpara.2011.01.005
[41]
Dubey JP, Lopez B, Alvarez M, Mendoza C, Lehmann T (2005) Isolation, tissue distribution, and molecular characterization of Toxoplasma gondii from free-range chickens from Guatemala. Parasitol 91: 955–957. doi: 10.1645/ge-493r.1
[42]
Ajzenberg D, Banuls AL, Su C, Dumetre A, Demar M, et al. (2004) Genetic diversity, clonality and sexuality in Toxoplasma gondii. Int J Parasitol 34: 1185–1196. doi: 10.1016/j.ijpara.2004.06.007
[43]
Dubey JP, Rajendran C, Costa DG, Ferreira LR, Kwok OC, et al. (2010) New Toxoplasma gondii genotypes isolated from free-range chickens from the Fernando de Noronha, Brazil: unexpected findings. J Parasitol 96: 709–712. doi: 10.1645/GE-2425.1
[44]
Meerburg B, Kijlstra A (2009) Changing climate—changing pathogens: Toxoplasma gondii in North-Western Europe. Parasitol Res 105: 17–24. doi: 10.1007/s00436-009-1447-4
[45]
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. American Journal of Tropical Medicine and Hygiene 77: 405–410.
[46]
Alford C Jr, Stagno S, Reynolds D (1974) Congenital toxoplasmosis: clinical, laboratory, and therapeutic considerations, with special reference to subclinical disease. Bull N Y Acad Med 50: 160–181.
[47]
Kimball AC, Kean BH, Fuchs F (1971) Congenital toxoplasmosis: a prospective study of 4,048 obstetric patients. Am J Obstet Gynecol 111: 211–218.
[48]
Wroblewski K, Meier P, Johnson V, Karrison T, McLeod R, et al. Estimates based on collections of data 1984-86 and 1986-88, age specific seroprevalence in pregnant women in two Chicago hospitals (The University of Chicago Hospitals and Michael Reese Hospital and Medical Center Papoz model).
[49]
Lopez A, Dietz VJ, Wilson M, Navin TR, Jones JL (2000) Preventing congenital toxoplasmosis.US Centers for Disease Control and Prevention. pp. 59–68.
[50]
Guerina NG, Hsu H, Meissner HC, Maguire JH, Lynfield R, et al. (1994) Neonatal serologic screening and early treatment for congenital toxoplasma gondii infection. New England Journal of Medicine 330: 1858–1863. doi: 10.1056/NEJM199406303302604
[51]
Gilbert RE, Thalib L, Hooi KT, Paul M, Wallon M, et al. (2007) Screening for congenital toxoplasmosis: Accuracy of immunoglobulin M and immunoglobulin A tests after birth. Journal of Medical Screening 14: 8–13. doi: 10.1258/096914107780154440
[52]
Naessens A, Jenum PA, Pollak A, Decoster A, Lappalainen M, 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
[53]
Isaac-Renton J, Bowie WR, King A, Irwin GS, Ong CS, et al. (1998) Detection of Toxoplasma gondii Oocysts in Drinking Water. Applied and Enviromental Microbiology 64: 2278–2280.
[54]
Benenson MW, Takafuji ET, Lemon SM, Greenup RL, Sulzer AJ (1982) Oocyst-transmitted toxoplasmosis associated with ingestion of contaminated water. N Engl J Med 307: 666–669. doi: 10.1056/NEJM198209093071107
[55]
Vaudaux JD, Muccioli C, James ER, Silveira C, Magargal SL, et al. (2010) Identification of an Atypical Strain of Toxoplasma gondii as the Cause of a Waterborne Outbreak of Toxoplasmosis in Santa Isabel do Ivai, Brazil. Journal of Infectious Diseases 202: 1226–1233. doi: 10.1086/656397
[56]
Montoya JG, Remington JS (2008) Management of Toxoplasma gondii Infection during Pregnancy. Clinical Infectious Diseases 554-566: doi: 10.1086/590149
[57]
Remington JS, McLeod R, Thulliez P, Desmonts G (2010) Toxoplasmosis. In: Remington J, Klein G, Wilson C, Baker C, editors. Infectious Disease of the Fetus and Newborn Infant 6th ed. Philadelphia: W.B. Saunders. pp. 947–1091.
[58]
Foulon W, Naessens A, Derde MP (1994) Evaluation of the possibilities for preventing congenital toxoplasmosis. American Journal of Perinatology 11: 57–62. doi: 10.1055/s-2007-994537
[59]
Boyer KM, Holfels E, Roizen N, S C, Mack D, et al. (2005) Risk factors for Toxoplasma gondii infection in mothers of infants with congenital toxoplasmosis: Implications for prenatal management and screening. American Journal of Obstetrics and Gynecology 192: 564–571. doi: 10.1016/j.ajog.2004.07.031
[60]
Couvreur J, Desmonts G, Thulliez P (1988) Prophylaxis of congenital toxoplasmosis. Effects of spiramycin on placental infection. Journal of Antimicrobial Chemotherapy 22: 193–200.
[61]
Scott RD II, Jones JL, Meltzer MI, Lopez A, Hsu H, et al. (2002) An Economic Analysis of Newborn Screening for Congenital Toxoplasmosis. Proceedings of the First Annual Meeting of the National Center for Birth Defects and Developmental Disabilities/CDC. Atlanta, GA: US Centers for Disease Control and Prevention.
[62]
Gilbert R (2009) Treatment for congenital toxoplasmosis: finding out what works. Mem Inst Oswaldo Cruz 104: 305–311. doi: 10.1590/S0074-02762009000200026
[63]
Chêne G, Thiébaut 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
[64]
Pinard JA, Leslie NS, Irvine PJ (2003) Maternal serologic screening for toxoplasmosis. Journal of Midwifery and Women's Health 48: 308–316. doi: 10.1016/s1526-9523(03)00279-4
[65]
Romand S, Chosson M, Franck J, Wallon M, Kieffer F, et al. (2004) Usefulness of quantitative polymerase chain reaction in amniotic fluid as early prognostic marker of fetal infection with Toxoplasma gondii. Am J Obstet Gynecol 190: 797–802. doi: 10.1016/j.ajog.2003.09.039
[66]
Daffos F, Forestier F, Capella-Pavlovsky M, Thulliez P, Aufrant C, et al. (1988) Prenatal management of 746 pregnancies at risk for congenital toxoplasmosis. New England Journal of Medicine 318: 271–275. doi: 10.1056/NEJM198802043180502
[67]
Villena I, Ancelle T, Delmas C, Garcia P, Brezin AP, et al. (2010) Congenital toxoplasmosis in France in 2007: first results from a national surveillance system. Euro Surveill 15: pii-19600.
[68]
Papoz L, Simondon F, Saurin W, Sarmini H (1986) A simple model relevant to toxoplasmosis applied to epidemiologic results in France. Am J Epidemiol. pp. 154–161.
[69]
Desmonts G, Couvreur J (1984) Congenital toxoplasmosis. Prospective study of the outcome of pregnancy in 542 women with toxoplasmosis acquired during pregnancy. Ann Pediatr (Paris) 31: 805–809.
[70]
Kodjikian L, Wallon M, Fleury M, Denis P, Binquet C, et al. (2006) Ocular manifestations in congenital toxoplasmosis. Graefes Arch Clin Exp Ophthalmol 244: 14–21. doi: 10.1007/s00417-005-1164-3
[71]
Couvreur J, Desmonts G, Aron-Rosa D (1984) Le prognostic oculare de la toxoplasmose congenitale: role du traitement. Ann Pediatr 31: 855–858.
[72]
Desmonts G (1982) Acquired toxoplasmosis in pregnant women. evaluation of the frequency of transmission of Toxoplasma and of congenital toxoplasmosis. Lyon Medical 248: 115–123.
[73]
Wallon M, Franck J, Thulliez P, Huissoud C, Peyron F, et al. (2010) Accuracy of real-time polymerase chain reaction for Toxoplasma gondii in amniotic fluid. Obstetrics and Gynecology 115: 727–733. doi: 10.1097/AOG.0b013e3181d57b09
[74]
Cahill A, Odibo A, Stamilio D, Macones G (2009) Screeening and treating for primary cytomegalovirus infection in pregnancy: where do we stand? A decision-analytic and economic analysis. American Journal of Obstetrics and Gynecology 201: 466.e461–467. doi: 10.1016/j.ajog.2009.07.056
[75]
Little S, Janakiraman V, Kaimal A, Musci T, Ecker J, et al. (2010) The cost-effectiveness of prenatal screening for spinal muscular atrophy. Am J Obstet Gynecol 202: 253.e251–257. doi: 10.1016/j.ajog.2010.01.032
[76]
Grosse S (2010) What is the value for money of prenatal carrier screening for spinal muscular atrophy? Too soon to say. Am J Obstet Gynecol 202: 209–211. doi: 10.1016/j.ajog.2010.01.031
[77]
Desmonts G, Couvreur J (1974) Toxoplasmosis in pregnancy and its transmission to the fetus. Bulletin of the New York Academy of Medicine: Journal of Urban Health 50: 146–159.
[78]
Forestier F (1991) Fetal disease, prenatal diagnosis and practical measures. Presse Med 1448–1454.
[79]
Stagno S, Reynolds DW, Amos CS, Dahle AJ, McCollister , et al. (1977) Auditory and visual defects resulting from symptomatic and subclinical congenital cytomegaloviral and Toxoplasma infections. Pediatrics 669–678.
[80]
Berrebi A, Bardou M, Bessieres M, Nowakowska D, Castagno R, et al. (2007) Outcome for children infected with congenital toxoplasmosis in the first trimester and with normal ultrasound findings: A study of 36 cases. European Journal of Obstetrics Gynecology and Reproductive Biology 135: 53–57. doi: 10.1016/j.ejogrb.2006.11.002
[81]
Honeycutt A, Dunlap L, Chen H, al Homsi G (2000) The Cost of Developmental Disabilities: Task Order No. 0621-09. Research Triangle Institute.
[82]
Lopez AD, Mathers CD, Ezzati M, Jamison D, Murray CJL (2006) Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. The Lancet 367: 1747–1757. doi: 10.1016/s0140-6736(06)68770-9
[83]
World Bank (1993) World Development Report 1993: Investing in Health. Oxford, UK: Oxford University Press.
[84]
Murray CJL, Lopez AD, editors. (1996) The Global Burden of Disease. Cambridge, MA: Harvard University Press.
[85]
Groot W, Maassen van den Brink H (2008) The value of health. BMC Health Services Research 8: doi: 10.1186/1472-6963-8-136
[86]
Landefeld JS, Seskin EP (1982) The Economic Value of Life: Linking Theory to Practice. American J of Public Health 72: 555–566. doi: 10.2105/ajph.72.6.555
[87]
Kruse M, Michelsen SI, Flachs EM, Br？nnum-Hansen H, Madsen M, Uldall P (2009) Lifetime costs of cerebral palsy. Developmental Medicine and Child Neurology 51: 622–628. doi: 10.1111/j.1469-8749.2008.03190.x
[88]
Nayer C (2009) The value of health in health reform. Drug Benefit Trends 21: 343–344.
[89]
Svensson M (2009) The value of a statistical life in Sweden: Estimates from two studies using the ‘Certainty Approach’ calibration. Accident Analysis and Prevention 430-437: doi: 10.1016/j.aap.2009.01.005
[90]
Mayo Clinic (2010) Amniocentesis. Mayo Clinic.
[91]
Olney RS, Moore CA, Khoury MJ, Erickson JD, Edmonds LD, et al. (1995) Chorionic villus sampling and amniocentesis: recommendations for prenatal counseling. MMWR Recomm Rep Centers for Disease Control and Prevention 44: 1–12.
[92]
Eddleman KA, Malone FD, Sullivan L, Dukes K, Berkowitz RL, et al. (2006) Pregnancy Loss Rates After Midtrimester Amniocentesis. American College of Obstetricians and Gynecologists 1067–1072.
[93]
Viscusi WK (2008) Value of life. In: Durlauf SN, Blume LE, editors. The New Palgrave Dictionary of Economics Online: Palgrave Macmillan.
[94]
McLeod R, Boyer KM, Lee D, Mui E, Wroblewski K, et al. (2011) Prematurity and Severity Associate with T. gondii Alleles. In submission, National Collaborative Congenital Toxoplasmosis Study NCCCTS, 1981–2009. doi: 10.1093/cid/cis258
[95]
Cornu C, Bissery A, Malbos C, Garwig R, Cocherel C, et al. (2009) Factors Affecting the Adherence to an Antenatal Screening Programme: An Experience with Toxoplasmosis Screening in France. Eurosurveillance 14: 1–5.
[96]
Wilson M, Remington JS, Clavet C, Varney G, Press C, et al. (1997) Evaluation of six commercial kits for detection of human immunoglobulin M antibodies to Toxoplasma gondii. Jnl Clin Microbiol 35: 3112–3115.
[97]
Calderaro A, Piccolo G, Peruzzi S, Gorrini C, Chezzi C, et al. (2008) Evaluation of Toxoplasma gondii Immunoglobulin G (IgG) and IgM Assays Incorporating the New Vidia Analyzer System. Clinical and Vaccine Immunology 15: 1076–1079. doi: 10.1128/CVI.00025-08
[98]
Mittendorf R, Pryde P, Herschel M, Williams MA (1999) Is routine antenatal toxoplasmosis screening justified in the United States? Statistical considerations in the application of medical screening tests. Clinical Obstetrics and Gynecology 42: 163–173. doi: 10.1097/00003081-199903000-00020
[99]
Bader TJ, Macones GA, Asch DA (1997) Prenatal screening for toxoplasmosis. Obstetrics and Gynecology 90: 457–464. doi: 10.1016/S0029-7844(97)00291-3
[100]
Boyer K, Hill D, Mui E, Wroblewski K, Karrison T, et al. (2011) Unrecognized ingestion of Toxopalsma gondii oocysts leads to congenital toxoplasmosis and causes epidemics in North America. Clin Inf Dis forthcoming.
[101]
Jara M, Ho Wen Hsu , Eaton RB, Demaria A (2001) Epidemiology of congenital toxoplasmosis identified by population-based newborn screening in Massachusetts. Pediatric Infectious Disease Journal 20: 1132–1135. doi: 10.1097/00006454-200112000-00007
[102]
Hohlfeld P, Daffos F, Costa J-M, Thulliez P, Forestier F, Vidaud M (1994) Prenatal diagnosis of congenital toxoplasmosis with a polymerase-chain-reaction test on amniotic fluid. N Engl J Med 695–699. doi: 10.1056/NEJM199409153311102
[103]
Liesenfeld O, Montoya JG, Kinney S, Press C, Remington SJ (2001) Effect of testing for IgG avidity in the diagnosis of Toxoplasma gondii infection in pregnant women: Experience in a US reference laboratory. Journal of Infectious Diseases 183: 1248–1253. doi: 10.1086/319672
