Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 26, Number 12—December 2020

Clinical and Multimodal Imaging Findings and Risk Factors for Ocular Involvement in a Presumed Waterborne Toxoplasmosis Outbreak, Brazil1

Camilo Brandão-de-Resende, Helena Hollanda Santos, Angel Alessio Rojas Lagos, Camila Munayert Lara, Jacqueline Souza Dutra Arruda, Ana Paula Maia Peixoto Marino, Lis Ribeiro do Valle Antonelli, Ricardo Tostes Gazzinelli, Ricardo Wagner de Almeida Vitor, and Daniel Vitor Vasconcelos-SantosComments to Author 
Author affiliations: Universidade Federal de Minas Gerais, Belo Horizonte, Brazil (C. Brandão-de-Resende, H.H. Santos, A.A.R. Lagos, C.M. Lara, J.S.D. Arruda, R.W.A, Vitor, D.V. Vasconcelos-Santos); Centro de Pesquisas René Rachou, Fundação Oswaldo Cruz, Belo Horizonte (A.P.M.P. Marino, L.R.V. Antonelli, R.T. Gazzinelli).

Main Article

Table 3

Ocular characteristics, recurrences, and complications of patients with ocular involvement from toxoplasmosis, Brazil*

Age, y/sex
Baseline eye examination
Follow-up findings
Last VA, mo; result
VA 0.0; SLE, AV cells and AC cells (0.5+/4+); FE, multifocal PR and peripheral large FNR
VA 0.0; SLE, AV cells; FE, PR
1 OD recurrence; month 2, satellite active lesion
21; 0.0 OU
VA 0.2; SLE, AV cells;FE, peripheral large FNR
VA 0.0; SLE, AV cells; FE, multiple peripheral large FNR
1 OD recurrence; month 22, new peripheral scar
Month 22, epiretinal membrane OD
34; 0.0 OU
40/M† Bilateral VA 0.0; SLE, AV cells; FE, multifocal PR VA 0.0; SLE, AV cells;
FE, multifocal PR and peripheral large FNR Multiple recurrences OU;
months 11, 21, and 24, active peripheral lesions; month 27, active peripheral lesion OS Month 21, epiretinal membrane OD; month 27, rhegmatogenous RD OS 36; 0.0 OD, 0.8 OS
VA 2.1; SL, EAV cells; FE, macular FNR
VA 0.3; SLE, AV cells;
FE, peripheral FNR
2 recurrences OS; new peripheral scar in months 12 and 15
Month 9, epiretinal membrane OD; month 34, epiretinal membrane OS
34; 1.9 OD, 0.4 OS
VA 0.0; SLE, normal; FE, Leber miliary aneurysms
VA 0.7; SLE, fine KP, AC cells 2+/4+, and AV cells; FE, peripheral large FNR

36; 0.1 OS
VA 0.0; SLE, AV cells; FE, PR
VA 0.0; normal SLE and FE

23; 0.0 OD
VA 0.5; SLE, granulomatous KP, AC cells (3+/4+), AV cells; IOP, 28 mmHg; FE, peripheral large FNR
VA 0.0; normal SLE and FE
1 recurrence OD; month 9, multiple active peripheral lesions OD
Baseline transient IOP elevation OD, 28mmHg
24; 0.0 OD
VA 0.0; normal SLE and FE
VA 0.0; SLE OS, AV cells; FE, multiple peripheral FNR

8; 0.0 OS
VA 0.5; SLE, AV cells;
FE, peripheral large FNR
VA 0.0; normal SLE and FE

Month 6, posterior vitreous detachment OD
37; 0.0 OD
VA 1.6; SLE, AV cells; FE, macular FNR
VA 0.0; normal SLE and FE

37; 1.9 OD
VA 0.0; SLE, AV cells; FE, peripheral large FNR
VA 0.0; normal SLE and FE

37; 0.0 OD
VA 0.0; SLE, AV cells; FE, PR
VA 0.0; normal SLE and FE

37; 0.0 OD
VA 0.0; normal SLE and FE
VA 0.0; normal SLE and FE
Late ocular involvement; OD VA 0.1; month 34, new peripheral scar
34; 0.1 OD
28/F‡ NA VA 0.0; normal SLE and FE VA 0.0; normal SLE and FE Late ocular involvement; OD VA 0.0; month 37, peripheral FNR None 39; 0.0 OD

*Age represents age at detection of first ocular lesion or scar. AC cells, grading of anterior chamber cells according to Standardization of Uveitis Nomenclature (SUN) working group (29); AV cells, anterior vitreous cells; FE, fundus examination; FNR, focal necrotizing retinochoroiditis, large FNR is >3 disk diameters; IOP, intraocular pressure; KP, keratic precipitates; NA, not applicable; OD, oculus dexter (right eye); OS, oculus sinister (left eye); OU, oculus uterque (both eyes); PR, punctate retinochoroiditis; RC, retinochoroiditis; RD, retinal detachment; SLE, slit-lamp examination; VA, visual acuity (log MAR); –, no recurrence or no new lesion.
†Patients with severe ocular involvement, including binocular, macular, or extensive necrotizing retinochoroiditis (>3 disk diameters).
‡Patients with initial normal ophthalmic examination.

Main Article

  1. Montoya  JG, Liesenfeld  O. Toxoplasmosis. Lancet. 2004;363:196576. DOIPubMedGoogle Scholar
  2. Holland  GN. Ocular toxoplasmosis: a global reassessment. Part I: epidemiology and course of disease. Am J Ophthalmol. 2003;136:97388. DOIPubMedGoogle Scholar
  3. Vasconcelos-Santos  DV. Ocular manifestations of systemic disease: toxoplasmosis. Curr Opin Ophthalmol. 2012;23:54350. DOIPubMedGoogle Scholar
  4. Aguirre  AA, Longcore  T, Barbieri  M, Dabritz  H, Hill  D, Klein  PN, et al. The One Health approach to toxoplasmosis: epidemiology, control, and prevention strategies. EcoHealth. 2019;16:37890. DOIPubMedGoogle Scholar
  5. Holland  GN. Ocular toxoplasmosis: a global reassessment. Part II: disease manifestations and management. Am J Ophthalmol. 2004;137:117. DOIPubMedGoogle Scholar
  6. Vasconcelos-Santos  DV, Machado Azevedo  DO, Campos  WR, Oréfice  F, Queiroz-Andrade  GM, Carellos  EVM, et al.; UFMG Congenital Toxoplasmosis Brazilian Group. Congenital toxoplasmosis in southeastern Brazil: results of early ophthalmologic examination of a large cohort of neonates. Ophthalmology. 2009;116:2199205.e1. DOIPubMedGoogle Scholar
  7. Arantes  TE, Silveira  C, Holland  GN, Muccioli  C, Yu  F, Jones  JL, et al. Ocular involvement following postnatally acquired Toxoplasma gondii infection in southern Brazil: a 28-year experience. Am J Ophthalmol. 2015;159:10021012.e2. DOIPubMedGoogle Scholar
  8. Holland  GN. Ocular toxoplasmosis: the influence of patient age. Mem Inst Oswaldo Cruz. 2009;104:3517. DOIPubMedGoogle Scholar
  9. Dadgostar  H, Silveira  C, Jones  JL, Lee  G, Muccioli  C, Belfort  R Jr, et al. Risk factors for ocular toxoplasmosis among individuals recently infected by Toxoplasma gondii in Southern Brazil. In: Abstracts of the Association for Research in Vision and Ophthalmology annual meeting. Invest Ophthalmol Vis Sci. 2008;49:5529.
  10. Portela  RW, Bethony  J, Costa  MI, Gazzinelli  A, Vitor  RW, Hermeto  FM, et al. A multihousehold study reveals a positive correlation between age, severity of ocular toxoplasmosis, and levels of glycoinositolphospholipid-specific immunoglobulin A. J Infect Dis. 2004;190:17583. DOIPubMedGoogle Scholar
  11. Bahia-Oliveira  LM, Jones  JL, Azevedo-Silva  J, Alves  CC, Oréfice  F, Addiss  DG. Highly endemic, waterborne toxoplasmosis in north Rio de Janeiro state, Brazil. Emerg Infect Dis. 2003;9:5562. DOIPubMedGoogle Scholar
  12. Balasundaram  MB, Andavar  R, Palaniswamy  M, Venkatapathy  N. Outbreak of acquired ocular toxoplasmosis involving 248 patients. Arch Ophthalmol. 2010;128:2832. DOIPubMedGoogle Scholar
  13. Bowie  WR, King  AS, Werker  DH, Isaac-Renton  JL, Bell  A, Eng  SB, et al.; The BC Toxoplasma Investigation Team. Outbreak of toxoplasmosis associated with municipal drinking water. Lancet. 1997;350:1737. DOIPubMedGoogle Scholar
  14. Burnett  AJ, Shortt  SG, Isaac-Renton  J, King  A, Werker  D, Bowie  WR. Multiple cases of acquired toxoplasmosis retinitis presenting in an outbreak. Ophthalmology. 1998;105:10327. DOIPubMedGoogle Scholar
  15. Silveira  C, Muccioli  C, Holland  GN, Jones  JL, Yu  F, de Paulo  A, et al. Ocular involvement following an epidemic of Toxoplasma gondii infection in Santa Isabel do Ivai, Brazil. Am J Ophthalmol. 2015;159:1013–21e3.
  16. Teutsch  SM, Juranek  DD, Sulzer  A, Dubey  JP, Sikes  RK. Epidemic toxoplasmosis associated with infected cats. N Engl J Med. 1979;300:6959. DOIPubMedGoogle Scholar
  17. Perkins  ES. Ocular toxoplasmosis. Br J Ophthalmol. 1973;57:117. DOIPubMedGoogle Scholar
  18. Benenson  MW, Takafuji  ET, Lemon  SM, Greenup  RL, Sulzer  AJ. Oocyst-transmitted toxoplasmosis associated with ingestion of contaminated water. N Engl J Med. 1982;307:6669. DOIPubMedGoogle Scholar
  19. Akstein  RB, Wilson  LA, Teutsch  SM. Acquired toxoplasmosis. Ophthalmology. 1982;89:1299302. DOIPubMedGoogle Scholar
  20. Malta  JMAS, Cabral  CM, Nóbrega  AA, Leite  PL, de Souza Alves  RM, Almeida  SML, et al. Outbreak of toxoplasmosis in the municipality of Gouveia, Minas Gerais [in Portuguese]. J Health Biol Sci. 2019;7:23341. DOIGoogle Scholar
  21. R: a language and environment for statistical computing. 2017; Vienna, Austria: R Foundation for Statistical Computing [cited 2020 Feb 2].
  22. Becker  S. A comparison of maximum likelihood and Jewell’s estimators of the odds ratio and relative risk in single 2 x 2 tables. Stat Med. 1989;8:98796. DOIPubMedGoogle Scholar
  23. Jabs  DA. Improving the reporting of clinical case series. Am J Ophthalmol. 2005;139:9005. DOIPubMedGoogle Scholar
  24. Harrington  DP, Fleming  TR. A class of rank test procedures for censored survival data. Biometrika. 1982;69:55366. DOIGoogle Scholar
  25. Mantel  N. Evaluation of survival data and two new rank order statistics arising in its consideration. Cancer Chemother Rep. 1966;50:16370.PubMedGoogle Scholar
  26. Bosch-Driessen  LE, Berendschot  TT, Ongkosuwito  JV, Rothova  A. Ocular toxoplasmosis: clinical features and prognosis of 154 patients. Ophthalmology. 2002;109:86978. DOIPubMedGoogle Scholar
  27. Labalette  P, Delhaes  L, Margaron  F, Fortier  B, Rouland  JF. Ocular toxoplasmosis after the fifth decade. Am J Ophthalmol. 2002;133:50615. DOIPubMedGoogle Scholar
  28. Johnson  MW, Greven  GM, Jaffe  GJ, Sudhalkar  H, Vine  AK. Atypical, severe toxoplasmic retinochoroiditis in elderly patients. Ophthalmology. 1997;104:4857. DOIPubMedGoogle Scholar
  29. Jabs  DA, Nussenblatt  RB, Rosenbaum  JT; Standardization of Uveitis Nomenclature (SUN) Working Group. Standardization of uveitis nomenclature for reporting clinical data. Results of the First International Workshop. Am J Ophthalmol. 2005;140:50916. DOIPubMedGoogle Scholar

Main Article

1Presented in part at the 2015 American Uveitis Society Fall meeting, November 15, 2014, Las Vegas, Nevada, USA

Page created: October 05, 2020
Page updated: November 19, 2020
Page reviewed: November 19, 2020
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.