Treatment of giardiasis: Current status and future directions topical collection on intra-abdominal infections, hepatitis, and gastroenteritis

Current Infectious Disease Reports

Volumn 16, Issue 2, 2014, Pages

  Watkins, Richard R ^a,b   Eckmann, Lars ^c  

^a Northeastern Ohio Medical University   (United States)

^b AKRON GENERAL MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Antibiotic development; Antibiotic resistance; Giardiasis; Vaccines

Indexed keywords

4 NITROIMIDAZOLE; AMINOGLYCOSIDE; ANTIINFECTIVE AGENT; ANTIPROTOZOAL AGENT; BENZIMIDAZOLE DERIVATIVE; NIRIDAZOLE; NITROFURAN; NITROFURAN DERIVATIVE; PROTOZOAL VACCINE; QUINOLINE DERIVATIVE;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL THERAPY; ARTICLE; GIARDIA; GIARDIASIS; HUMAN; NONHUMAN; PATHOGENESIS; VACCINATION;

EID: 84895513780     PISSN: 15233847     EISSN: 15343146     Source Type: Journal    
DOI: 10.1007/s11908-014-0396-y     Document Type: Article

References (62)

1. Thomas IV LJ, Zweig AP, Tosh AK. An adolescent with chronic giardiasis mimicking anorexia nervosa. Int J Adolesc Med Health. 2013. doi: 10.1515/ijamh-2013-0506.
2. Wensaas KA, Langeland N, Hanevik K, et al. Irritable bowel syndrome and chronic fatigue 3 years after acute giardiasis: historic cohort study. Gut. 2012;61:214-9.
3. Upcroft P, Upcroft JA. Drug targets and mechanisms of resistance in anaerobic protozoa. Clin Microbiol Rev. 2001;14:150-64.
4. Tejman-Yarden N, Millman M, Lauwaet T, et al. Impaired parasite attachment as fitness cost of metronidazole resistance in Giardia lamblia. Antimicrob Agents Chemother. 2011;55:4643-51.
5. Abboud P, Lemée V, Gargala G, et al. Successful treatment of metronidazole- and albendazole-resistant giardiasis with nitazoxanide in a patient with acquired immunodeficiency syndrome. Clin Infect Dis. 2001;32:1792-4.
6. Escobedo AA, Cimerman S. Giardiasis: a pharmacotherapy review. Expert Opin Pharmacother. 2007;8:1885-902.
7. Samuelson J. Why metronidazole is active against both bacteria and parasites. Antimicrob Agents Chemother. 1999;43:1533-41.
8. Hoffman PS, Sisson G, Croxen MA, et al. Antiparasitic drug nitazoxanide inhibits the pyruvate oxidoreductases of Helicobacter pylori, selected anaerobic bacteria and parasites, and Campylobacter jejuni. Antimicrob Agents Chemother. 2007;51:868-76.
9. Rossignol JF, Lopez-Chegne N, Julcamoro LM, et al. Nitazoxanide for the empiric treatment of pediatric infectious diarrhea. Trans R Soc Trop Med Hyg. 2012;106:167-73.
10. Jiang X, Sun L, Qiu JJ, et al. A novel application of furazolidone: anti-leukemic activity in acute myeloid leukemia. PLoS One. 2013;8:e72335.
11. Solaymani-Mohammadi S, Genkinger JM, Loffredo CA, Singer SM. A meta-analysis of the effectiveness of albendazole compared with metronidazole as treatments for infections with Giardia duodenalis. PLoS Negl Trop Dis. 2010;4(5):e682.
12. Cañete R, Rodríguez P, Mesa L, et al. Albendazole versus metronidazole in the treatment of adult giardiasis: a randomized, double-blind, clinical trial. Curr Med Res Opin. 2012;28:149-54.
13. Granados CE, Reveiz L, Uribe LG, Criollo CP. Drugs for treating giardiasis. Cochrane Database Syst Rev. 2012;12:CD007787. A review of 19 randomized controlled trials involving 1,817 patients that compared metronidazole to alternative therapy; albendazole had similar efficacy with fewer side effects and a simplified regimen.
14. Blackwell AD, Martin M, Kaplan H, Gurven M. Antagonism between two intestinal parasites in humans: the importance of co-infection for infection risk and recovery dynamics. Proc Biol Sci. 2013;280:20131671.
15. Requena-Méndez A, Goñi P, Lóbez S, et al. A family cluster of giardiasis with variable treatment responses: refractory giardiasis in a family after a trip to India. Clin Microbiol Infect. 2014;20:O135-8.
16. Escobedo AA, Núñez FA, Moreira I, et al. Comparison of chloroquine, albendazole and tinidazole in the treatment of children with giardiasis. Ann Trop Med Parasitol. 2003;97:367-71.
17. Cañete R, Rivas DE, Escobedo AA, et al. A randomized, controlled, open-label trial evaluating the efficacy and safety of chloroquine in the treatment of giardiasis in children. West Indian Med J. 2010;59:607-11.
18. Mørch K, Hanevik K, Robertson LJ, et al. Treatment-ladder and genetic characterisation of parasites in refractory giardiasis after an outbreak in Norway. J Infect. 2008;56:268-73.
19. Lopez-Velez R, Batlle C, Jiménez C, et al. Short course combination therapy for giardiasis after nitroimidazole failure. Am J Trop Med Hyg. 2010;83:171-3.
20. Lalle M. Giardiasis in the post genomic era: treatment, drug resistance and novel therapeutic perspectives. Infect Disord Drug Targets. 2010;10:283-94.
21. Dan M, Wang AL, Wang CC. Inhibition of pyruvate-ferredoxin oxidoreductase gene expression in Giardia lamblia by a virus-mediated hammerhead ribozyme. Mol Microbiol. 2000;36(2):447-56.
22. Townson SM, Upcroft JA, Upcroft P. Characterisation and purification of pyruvate:ferredoxin oxidoreductase from Giardia duodenalis. Mol Biochem Parasitol. 1996;79:183-93.
23. Leitsch D, Burgess AG, Dunn LA, et al. Pyruvate:ferredoxin oxidoreductase and thioredoxin reductase are involved in 5-nitroimidazole activation while flavin metabolism is linked to 5-nitroimidazole resistance in Giardia lamblia. J Antimicrob Chemother. 2011;66:1756-65.
24. Müller J, Ley S, Felger I, Hemphill A, Müller N. Identification of differentially expressed genes in a Giardia lamblia WB C6 clone resistant to nitazoxanide and metronidazole. J Antimicrob Chemother. 2008;62:72-82.
25. Aguayo-Ortiz R, Méndez-Lucio O, Romo-Mancillas A, et al. Molecular basis for benzimidazole resistance from a novel β-tubulin binding site model. J Mol Graph Model. 2013;45C:26-37.
26. Valdez CA, Tripp JC, Miyamoto Y, et al. Synthesis and electrochemistry of 2-ethenyl and 2-ethanyl derivatives of 5-nitroimidazole and antimicrobial activity against Giardia lamblia. J Med Chem. 2009;52:4038-53.
27. Upcroft JA, Dunn LA, Wright JM, et al. 5-Nitroimidazole drugs effective against metronidazole-resistant Trichomonas vaginalis and Giardia duodenalis. Antimicrob Agents Chemother. 2006;50:344-7.
28. Nillius D, Müller J, Müller N. Nitroreductase (GlNR1) increases susceptibility of Giardia lamblia and Escherichia coli to nitro drugs. J Antimicrob Chemother. 2011;66:1029-35.
29. Müller J, Schildknecht P, Müller N. Metabolism of nitro drugs metronidazole and nitazoxanide in Giardia lamblia: characterization of a novel nitroreductase (GlNR2). J Antimicrob Chemother. 2013;68:1781-9.
30. Busatti HG, Alves RJ, Santana-Anjos KG, et al. Effects of metronidazole analogues on Giardia lamblia: experimental infection and cell organization. Diagn Microbiol Infect Dis. 2013;75:160-4.
31. Navarrete-Vazquez G, Chávez-Silva F, Argotte-Ramos R, et al. Synthesis of benzologues of nitazoxanide and tizoxanide: a comparative study of their in vitro broad-spectrum antiprotozoal activity. Bioorg Med Chem Lett. 2011;21:3168-71.
32. Miyamoto Y, Kalisiak J, Korthals K, et al. Expanded therapeutic potential in activity space of next-generation 5-nitroimidazole antimicrobials with broad structural diversity. Proc Natl Acad Sci U S A. 2013;110:17564-9. This paper describes a novel approach to the synthesis of 5-NI drugs with greatly enhanced activity against a number of important pathogens including pathogenic protozoa. These compounds can overcome different forms of drug resistance and are nontoxic in animal models.
33. Pérez-Villanueva J, Hernández-Campos A, Yépez-Mulia L, et al. Synthesis and antiprotozoal activity of novel 2-{[2-(1H-imidazol-1-yl) ethyl]sulfanyl}-1H-benzimidazole derivatives. Bioorg Med Chem Lett. 2013;23:4221-4.
34. Mavrova AT, Vuchev D, Anichina K, Vassilev N. Synthesis, antitrichinnellosis and antiprotozoal activity of some novel thieno[2,3-d]pyrimidin-4(3H)-ones containing benzimidazole ring. Eur J Med Chem. 2010;45:5856-61.
35. Hernández-Covarrubias C, Vilchis-Reyes MA, Yépez-Mulia L, et al. Exploring the interplay of physicochemical properties, membrane permeability and giardicidal activity of some benzimidazole derivatives. Eur J Med Chem. 2012;52:193-204.
36. Pérez-Villanueva J, Santos R, Hernández-Campos A, et al. Towards a systematic characterization of the antiprotozoal activity landscape of benzimidazole derivatives. Bioorg Med Chem. 2010;18:7380-91.
37. Torres-Gómez H, Hernández-Núñez E, León-Rivera I, et al. Design, synthesis and in vitro antiprotozoal activity of benzimidazole-pentamidine hybrids. Bioorg Med Chem Lett. 2008;18:3147-51.
38. Nava-Zuazo C, Estrada-Soto S, Guerrero-Alvarez J, et al. Design, synthesis, and in vitro antiprotozoal, antimycobacterial activities of N-{2-[(7-chloroquinolin-4-yl)amino]ethyl}ureas. Bioorg Med Chem. 2010;18:6398-403.
39. Tejman-Yarden N, Miyamoto Y, Leitsch D, et al. A reprofiled drug, auranofin, is effective against metronidazole-resistant Giardia lamblia. Antimicrob Agents Chemother. 2013;57:2029-35. Auranofin demonstrated in vivo and in vitro antigiardial activity, including against metronidazole-resistant strains.
40. Chen CZ, Southall N, Galkin A, et al. A homogenous luminescence assay reveals novel inhibitors for Giardia lamblia carbamate kinase. Curr Chem Genomics. 2012;6:93-102.
41. Manna D, Dutta PK, Achari B, Lohia A. A novel galacto-glycerolipid from Oxalis corniculata kills Entamoeba histolytica and Giardia lamblia. Antimicrob Agents Chemother. 2010;54:4825-32.
42. Al-Jaber HI, Mosleh IM, Mallouh A, et al. Chemical constituents of Osyris alba and their antiparasitic activities. J Asian Nat Prod Res. 2010;12:814-20.
43. Rahimi-Esboei B, Ebrahimzadeh MA, Gholami S, Falah-Omrani V. Anti-giardial activity of Sambucus ebulus. Eur Rev Med Pharmacol Sci. 2013;17:2047-50.
44. Johnston BC, Ma SS, Goldenberg JZ, et al. Probiotics for the prevention of Clostridium difficile-associated diarrhea: a systematic review and meta-analysis. Ann Intern Med. 2012;157:878-88.
45. Singer SM, Nash TE. The role of normal flora in Giardia lamblia infections in mice. J Infect Dis. 2000;181:1510-2.
46. Shukla G, Kaur H, Sharma L. Comparative therapeutic effect of probiotic Lactobacillus casei alone and in conjunction with antiprotozoal drugs in murine giardiasis. Parasitol Res. 2013;112:2143-9.
47. Kridel SJ, Axelrod F, Rozenkrantz N, Smith JW. Orlistat is a novel inhibitor of fatty acid synthase with antitumor activity. Cancer Res. 2004;64(6):2070-5.
48. Yuan J, Cheng KC, Johnson RL, et al. Chemical genomic profiling for antimalarial therapies, response signatures, and molecular targets. Science. 2011;333:724-9.
49. Hahn J, Seeber F, Kolodziej H, et al. High sensitivity of Giardia duodenalis to tetrahydrolipstatin (orlistat) in vitro. PLoS One. 2013;8:e71597. Orlistat inhibited in vitro growth of Giardia much more effectively than metronidazole and there was no demonstrated antagonism between the two agents, suggesting a potential combination therapy.
50. Eissa MM, Amer EI. Giardia lamblia: a new target for miltefosine. Int J Parasitol. 2012;42:443-52. Miltefosine is an antileishmanial drug that in a mouse model induced severe morphological changes in Giardia trophozoites.
51. Tejman-Yarden N, Eckmann L. New approaches to the treatment of giardiasis. Curr Opin Infect Dis. 2011;24:451-6.
52. Eckmann L, Laurent F, Langford TD, et al. Nitric oxide production by human intestinal epithelial cells and competition for arginine as potential determinants of host defense against the lumen-dwelling pathogen Giardia lamblia. J Immunol. 2000;164:1478-87.
53. Banik S, Renner Viveros P, Seeber F, et al. Giardia duodenalis arginine deiminase modulates the phenotype and cytokine secretion of human dendritic cells by depletion of arginine and formation of ammonia. Infect Immun. 2013;81:2309-17.
54. Li Z, Kulakova L, Li L, et al. Mechanisms of catalysis and inhibition operative in the arginine deiminase from the human pathogen Giardia lamblia. Bioorg Chem. 2009;37:149-61.
55. Leibly DJ, Newling PA, Abendroth J, et al. Structure of a cyclin-dependent kinase from Giardia lamblia. Acta Crystallogr Sect F: Struct Biol Cryst Commun. 2011;67(Pt 9):1084-9.
56. Hernández-Alcántara G, Torres-Larios A, Enríquez-Flores S, et al. Structural and functional perturbation of Giardia lamblia triosephosphate isomerase by modification of a non-catalytic, non-conserved region. PLoS One. 2013;8:e69031.
57. Li Z, Liu Z, Cho DW, et al. Rational design, synthesis and evaluation of first generation inhibitors of the Giardia lamblia fructose-1,6-biphosphate aldolase. J Inorg Biochem. 2011;105(4):509-17.
58. Han J, Collins LJ. Reconstruction of sugar metabolic pathways of Giardia lamblia. Int J Proteomics. 2012;2012:980829.
59. Olson ME, Ceri H, Morck DW. Giardia vaccination. Parasitol Today. 2000;16:213-7.
60. Olson ME, Hannigan CJ, Gaviller PF, Fulton LA. The use of a Giardia vaccine as an immunotherapeutic agent in dogs. Can Vet J. 2001;42:865-8.
61. Jenikova G, Hruz P, Andersson MK, et al. 1-giardin based live heterologous vaccine protects against Giardia lamblia infection in a murine model. Vaccine. 2011;29:9529-37. The conserved antigen α1-giardin was significantly immunogenic in a mouse model of giardiasis and induced protection against subsequent Giardia challenge; this suggests it could be a suitable candidate antigen for a vaccine against giardiasis.
62. Prucca CG, Rivero FD, Luján HD. Regulation of antigenic variation in Giardia lamblia. Annu Rev Microbiol. 2011;65:611-30.