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 27, Number 7—July 2021
Research

Triclabendazole Treatment Failure for Fasciola hepatica Infection among Preschool and School-Age Children, Cusco, Peru1

Maria L. Morales, Melinda B. Tanabe, A. Clinton White, Martha Lopez, Ruben Bascope, and Miguel M. CabadaComments to Author 
Author affiliations: Universidad Peruana Cayetano Heredia, Cusco, Peru (M.L. Morales, A.C. White Jr., M. Lopez, M.M. Cabada); University of Texas Medical Branch, Galveston, Texas, USA (M.B. Tanabe, A.C. White Jr., M.M. Cabada); Peruvian Ministry of Health, Cusco (R. Bascope)

Main Article

Table 3

Response to first round of triclabendazole treatment for Fasciola hepatica infection among preschool and school-age children compared with failure to respond to first or fourth round of treatment, Cusco, Peru*

Characteristic Cured after first round, n = 80 Failed after first round, n = 66 p value† Failed after fourth round, n = 17 p value†
District
Anta 27 (34) 26 (39) 0.48 12 (71) 0.005
Other
53 (64)
40 (61)

5 (29)

Fas2 ELISA result
Negative 27 (35) 12 (18) 0.02 2 (12) 0.08
Positive
50 (65)
54 (82)

15 (88)

Likelihood of poverty‡
<50% 56 (70) 56 (89) 0.08 17 (100) 0.03
>50%
16 (30)
7 (11)

0 (0)

Other parasites§
No 42 (53) 41 (62) 0.24 11 (65) 0.35
Yes
38 (48)
25 (38)

6 (35)

Sex
F 44 (55) 33 (50) 0.54 10 (59) 0.77
M
36 (45)
33 (50)

7 (41)

Age, y, mean ± SD
10.5 ± 2.9
10.4 ± 3.4
0.85
9.0 ± 3.6
0.06
Baseline egg count, eggs/g of stool 33.3 (6.6–53.3) 48.3 (25–87.5) 0.001 60 (26–100) 0.005
Baseline hemoglobin, g/dL¶ 12.9 (12.1–13.7) 12.9 (12.3–13.4) 0.97 12.3 (12–13) 0.08
Baseline HAZ# −1.6 (−2.2 to −1.0)# −1.5 (−2.0 to −0.9)# 0.19 −1.2 (−1.9 to −0.7) 0.17
Eosinophil count, cells/μL 300 (190–460)# 265 (197–412) 0.36 310 (230–500) 0.64

*Values are no. (%) or median (interquartile range) except as indicated. HAZ, height-for-age Z score. †By Mann-Whitney U test. ‡Likelihood of living under US $3.75/day poverty line (18). §Gastrointestinal parasites. ¶Uncorrected at enrollment. #One or 2 persons were missing information for this variable.

Main Article

References
  1. World Health Organization. Fascioliasis diagnosis, treatment and control strategy (updated 2014) [cited 2020 May 28]. https://www.who.int/foodborne_trematode_infections/fascioliasis/fascioliasis_diagnosis
  2. Wessely  K, Reischig  HL, Heinerman  M, Stempka  R. Human fascioliasis treated with triclabendazole (Fasinex) for the first time. Trans R Soc Trop Med Hyg. 1988;82:7434. DOIPubMedGoogle Scholar
  3. Villegas  F, Angles  R, Barrientos  R, Barrios  G, Valero  MA, Hamed  K, et al. Administration of triclabendazole is safe and effective in controlling fascioliasis in an endemic community of the Bolivian Altiplano. PLoS Negl Trop Dis. 2012;6:e1720. DOIPubMedGoogle Scholar
  4. el-Morshedy  H, Farghaly  A, Sharaf  S, Abou-Basha  L, Barakat  R. Triclabendazole in the treatment of human fascioliasis: a community-based study. East Mediterr Health J. 1999;5:88894.PubMedGoogle Scholar
  5. Maco  V, Marcos  L, Delgado  J, Herrera  J, Nestares  J, Terashima  A, et al. Efficacy and tolerability of two single-day regimens of triclabendazole for fascioliasis in Peruvian children. Rev Soc Bras Med Trop. 2015;48:44553. DOIPubMedGoogle Scholar
  6. Centers for Disease Control and Prevention. Fasciola. Resources for health professionals and treatment (updated 2019) [cited 2020 May 28]. https://www.cdc.gov/parasites/fasciola/health_professionals/index.html
  7. Talaie  H, Emami  H, Yadegarinia  D, Nava-Ocampo  AA, Massoud  J, Azmoudeh  M, et al. Randomized trial of a single, double and triple dose of 10 mg/kg of a human formulation of triclabendazole in patients with fascioliasis. Clin Exp Pharmacol Physiol. 2004;31:77782. DOIPubMedGoogle Scholar
  8. US Food and Drug Administration. Drug approval package: Egaten (triclabendazole) 2019 [cited 2020 May 28]. https://www.accessdata.fda.gov/drugsatfda_docs/nda/2018/208711Orig1s000TOC.cfm
  9. Mollinedo  S, Gutierrez  P, Azurduy  R, Valle  F, Salas  A, Mollinedo  Z, et al. Mass drug administration of triclabendazole for Fasciola hepatica in Bolivia. Am J Trop Med Hyg. 2019;100:14947. DOIPubMedGoogle Scholar
  10. Bayhan  GI, Özkan  AT, Beyhan  YE. The clinical characteristics of fascioliasis in pediatric patients. Turk Pediatri Ars. 2020;55:6771.PubMedGoogle Scholar
  11. Overend  DJ, Bowen  FL. Resistance of Fasciola hepatica to triclabendazole. Aust Vet J. 1995;72:2756. DOIPubMedGoogle Scholar
  12. Kelley  JM, Elliott  TP, Beddoe  T, Anderson  G, Skuce  P, Spithill  TW. Current threat of triclabendazole resistance in Fasciola hepatica. Trends Parasitol. 2016;32:45869. DOIPubMedGoogle Scholar
  13. Winkelhagen  AJ, Mank  T, de Vries  PJ, Soetekouw  R. Apparent triclabendazole-resistant human Fasciola hepatica infection, the Netherlands. Emerg Infect Dis. 2012;18:10289. DOIPubMedGoogle Scholar
  14. Cabada  MM, Lopez  M, Cruz  M, Delgado  JR, Hill  V, White  AC Jr. Treatment failure after multiple courses of triclabendazole among patients with fascioliasis in Cusco, Peru: a case series. PLoS Negl Trop Dis. 2016;10:e0004361. DOIPubMedGoogle Scholar
  15. Branco  EA, Ruas  R, Nuak  J, Sarmento  A. Treatment failure after multiple courses of triclabendazole in a Portuguese patient with fascioliasis. BMJ Case Rep. 2020;13:e232299. DOIPubMedGoogle Scholar
  16. Cabada  MM, Morales  ML, Webb  CM, Yang  L, Bravenec  CA, Lopez  M, et al. Socioeconomic factors associated with Fasciola hepatica infection among children from 26 communities of the Cusco region of Peru. Am J Trop Med Hyg. 2018;99:11805. DOIPubMedGoogle Scholar
  17. Lopez  M, Morales  ML, Konana  M, Hoyer  P, Pineda-Reyes  R, White  AC Jr, et al. Kato-Katz and Lumbreras rapid sedimentation test to evaluate helminth prevalence in the setting of a school-based deworming program. Pathog Glob Health. 2016;110:1304. DOIPubMedGoogle Scholar
  18. Schreiner  M. A simple poverty scorecard for Peru 2009 [cited 2021 Jan 14]. https://www.simplepovertyscorecard.com/PER_2007_ENG.pdf
  19. Keiser  J, Engels  D, Büscher  G, Utzinger  J. Triclabendazole for the treatment of fascioliasis and paragonimiasis. Expert Opin Investig Drugs. 2005;14:151326. DOIPubMedGoogle Scholar
  20. Black  CL, Steinauer  ML, Mwinzi  PN, Evan Secor  W, Karanja  DM, Colley  DG. Impact of intense, longitudinal retreatment with praziquantel on cure rates of schistosomiasis mansoni in a cohort of occupationally exposed adults in western Kenya. Trop Med Int Health. 2009;14:4507. DOIPubMedGoogle Scholar
  21. Esteban  JG, Flores  A, Angles  R, Mas-Coma  S. High endemicity of human fascioliasis between Lake Titicaca and La Paz valley, Bolivia. Trans R Soc Trop Med Hyg. 1999;93:1516. DOIPubMedGoogle Scholar
  22. Duthaler  U, Smith  TA, Keiser  J. In vivo and in vitro sensitivity of Fasciola hepatica to triclabendazole combined with artesunate, artemether, or OZ78. Antimicrob Agents Chemother. 2010;54:4596604. DOIPubMedGoogle Scholar
  23. Ramadan  HK, Hassan  WA, Elossily  NA, Ahmad  AA, Mohamed  AA, Abd-Elkader  AS, et al. Evaluation of nitazoxanide treatment following triclabendazole failure in an outbreak of human fascioliasis in Upper Egypt. PLoS Negl Trop Dis. 2019;13:e0007779. DOIPubMedGoogle Scholar
  24. Chen  JX, Chen  MX, Ai  L, Xu  XN, Jiao  JM, Zhu  TJ, et al. An outbreak of human fascioliasis gigantica in Southwest China. PLoS One. 2013;8:e71520. DOIPubMedGoogle Scholar
  25. Instituto Nacional de Estadistica e Informatica. Provincial and district poverty map, 2013. Lima, Peru [in Spanish] [cited 2020 May 28]. https://www.inei.gob.pe/media/MenuRecursivo/publicaciones_digitales/Est/Lib1261/Libro.pdf
  26. Sargison  ND, Scott  PR. Diagnosis and economic consequences of triclabendazole resistance in Fasciola hepatica in a sheep flock in south-east Scotland. Vet Rec. 2011;168:159. DOIPubMedGoogle Scholar
  27. Webster  JP, Molyneux  DH, Hotez  PJ, Fenwick  A. The contribution of mass drug administration to global health: past, present and future. Philos Trans R Soc Lond B Biol Sci. 2014;369:20130434. DOIPubMedGoogle Scholar
  28. Lukambagire  AH, Mchaile  DN, Nyindo  M. Diagnosis of human fascioliasis in Arusha region, northern Tanzania by microscopy and clinical manifestations in patients. BMC Infect Dis. 2015;15:578. DOIPubMedGoogle Scholar
  29. Zumaquero-Ríos  JL, Sarracent-Pérez  J, Rojas-García  R, Rojas-Rivero  L, Martínez-Tovilla  Y, Valero  MA, et al. Fascioliasis and intestinal parasitoses affecting schoolchildren in Atlixco, Puebla State, Mexico: epidemiology and treatment with nitazoxanide. PLoS Negl Trop Dis. 2013;7:e2553. DOIPubMedGoogle Scholar

Main Article

1Preliminary results from this study were presented at the 68th Annual Meeting of the American Society of Tropical Medicine and Hygiene, November 20‒24, 2019, National Harbor, MD, USA.

Page created: April 26, 2021
Page updated: June 16, 2021
Page reviewed: June 16, 2021
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.
file_external