Efficacy of three-week oxytetracycline or rifampin monotherapy compared with a combination regimen against the filarial nematode Onchocerca ochengi

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 2, 2014, Pages 801-810

  Bah, Germanus S ^a,c   Ward, Emma L ^a   Srivastava, Abhishek ^b,d   Trees, Alexander J ^a,b   Tanya, Vincent N ^c   Makepeace, Benjamin L ^a,b  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^c Regional Centre of Wakwa   (Cameroon)

^d Abhishek Srivastava   (India)

Author keywords

[No Author keywords available]

Indexed keywords

OXYTETRACYCLINE; RIFAMPICIN; TERRAMYCIN LA; UNCLASSIFIED DRUG;

AFRICA SOUTH OF THE SAHARA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOAVAILABILITY; BOS INDICUS; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DERMATITIS; DRUG BLOOD LEVEL; FEMALE; HELMINTHIASIS; MALE; MINIMUM INHIBITORY CONCENTRATION; MONOTHERAPY; NONHUMAN; ONCHOCERCA; ONCHOCERCA OCHENGI; ONCHOCERCIASIS; PRIORITY JOURNAL; VISUAL IMPAIRMENT; WOLBACHIA;

ADULT; ANIMALS; ANTI-BACTERIAL AGENTS; CATTLE; DRUG ADMINISTRATION SCHEDULE; DRUG COMBINATIONS; HUMANS; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; ONCHOCERCA; ONCHOCERCIASIS; OXYTETRACYCLINE; PARASITE LOAD; RIFAMPIN; SKIN; SYMBIOSIS; TREATMENT OUTCOME; WOLBACHIA;

EID: 84893490805     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01995-13     Document Type: Article

References (50)

1. Anonymous. 2010. Onchocerciasis (river blindness), p 123-128. In CromptonDWT,Peters P (ed), Working to overcome the global impact of neglected tropical diseases: first WHO report on neglected tropical diseases. World Health Organization, Geneva, Switzerland.
2. Plaisier AP, Van Oortmarssen GJ, Remme J, Habbema JD. 1991. The reproductive lifespan of Onchocerca volvulus in West African savanna. Acta Trop. 48:271-284. http://dx.doi.org/10.1016/0001-706X(91)90015-C.
3. Schulz-Key H. 1990. Observations on the reproductive biology of Onchocerca volvulus. Acta Leiden 59:27-44.
4. Crump A, Morel CM, Omura S. 2012. The onchocerciasis chronicle: from the beginning to the end? Trends Parasitol. 28:280-288. http://dx.doi.org/10.1016/j. pt.2012.04.005.
5. Tielsch JM, Beeche A. 2004. Impact of ivermectin on illness and disability associated with onchocerciasis. Trop. Med. Int. Health 9:A45-A56. http://dx.doi.org/10.1111/j.1365-3156.2004.01213.x.
6. Traore MO, Sarr MD, Badji A, Bissan Y, Diawara L, Doumbia K, Goita SF, Konate L, Mounkoro K, Seck AF, Toe L, Toure S, Remme JH. 2012. Proof-of-principle of onchocerciasis elimination with ivermectin treatment in endemic foci in Africa: final results of a study in Mali and Senegal. PLoS Negl. Trop. Dis. 6:e1825. http://dx.doi.org/10.1371/journal.pntd.0001825.
7. Gardon J, Gardon-Wendel N, Demanga N, Kamgno J, Chippaux JP, Boussinesq M. 1997. Serious reactions after mass treatment of onchocerciasis with ivermectin in an area endemic for Loa loa infection. Lancet 350:18-22. http://dx.doi.org/10.1016/S0140-6736(96)11094-1.
8. Katabarwa MN, Lakwo T, Habomugisha P, Agunyo S, Byamukama E, Oguttu D, Tukesiga E, Unoba D, Dramuke P, Onapa A, Tukahebwa EM, Lwamafa D, Walsh F, Unnasch TR. 2013. Transmission of Onchocerca volvulus continues in Nyagak-Bondo focus of northwestern Uganda after 18 years of a single dose of annual treatment with ivermectin. Am. J. Trop. Med. Hyg. 89:293-300. http://dx.doi.org/10.4269/ ajtmh.13-0037.
9. Katabarwa MN, Eyamba A, Nwane P, Enyong P, Kamgno J, Kuete T, Yaya S, Aboutou R, Mukenge L, Kafando C, Siaka C, Mkpouwoueiko S, Ngangue D, Biholong BD, Andze GO. 2013. Fifteen years of annual mass treatment of onchocerciasis with ivermectin have not interrupted transmission in the west region of Cameroon. J. Parasitol. Res. 2013:420928. http://dx.doi.org/10.1155/2013/420928.
10. Osei-Atweneboana MY, Eng Boakye JKDA, Gyapong JO, Prichard RK. 2007. Prevalence and intensity of Onchocerca volvulus infection and efficacy of ivermectin in endemic communities in Ghana: a two-phase epidemiological study. Lancet 369:2021-2029. http://dx.doi.org/10.1016/S0140-6736(07)60942-8.
11. Osei-Atweneboana MY, Awadzi K, Attah SK, Boakye DA, Gyapong JO, Prichard RK. 2011. Phenotypic evidence of emerging ivermectin resistance in Onchocerca volvulus. PLoS Negl. Trop. Dis. 5:e998. http://dx.doi.org/10.1371/journal.pntd. 0000998.
12. Brieger WR, Okeibunor JC, Abiose AO, Ndyomugyenyi R, Wanji S, Elhassan E, Amazigo UV. 2012. Characteristics of persons who complied with and failed to comply with annual ivermectin treatment. Trop. Med. Int. Health 17:920-930. http://dx.doi.org/10.1111/j.1365-3156.2012.03007.x.
13. Awadzi K, Attah SK, Addy ET, Opoku NO, Quartey BT. 1999. The effects of high-dose ivermectin regimens on Onchocerca volvulus in onchocerciasis patients. Trans. R. Soc. Trop. Med. Hyg. 93:189-194. http://dx.doi.org/10.1016/S0035- 9203(99)90305-X.
14. Taylor MJ, Bilo K, Cross HF, Archer JP, Underwood AP. 1999. 16S rDNA phylogeny and ultrastructural characterization of Wolbachia intracellular bacteria of the filarial nematodes Brugia malayi, B. pahangi, and Wuchereria bancrofti. Exp. Parasitol. 91:356-361. http://dx.doi.org/10.1006/expr.1998.4383.
15. Henkle-Dührsen K, Eckelt VH, Wildenburg G, Blaxter M, Walter RD. 1998. Gene structure, activity and localization of a catalase from intracellular bacteria in Onchocerca volvulus. Mol. Biochem. Parasitol. 96:69-81. http://dx.doi.org/10.1016/S0166-6851(98)00109-1.
16. Hoerauf A, Nissen-Pähle K, Schmetz C, Henkle-Dührsen K, Blaxter ML, Büttner DW, Gallin MY, Al-Qaoud KM, Lucius R, Fleischer B. 1999. Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility. J. Clin. Invest. 103:11-18. http://dx.doi.org/10.1172/JCI4768.
17. Bandi C, McCall JW, Genchi C, Corona S, Venco L, Sacchi L. 1999. Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia. Int. J. Parasitol. 29:357-364. http://dx.doi.org/10.1016/S0020-7519(98)00200-8.
18. Langworthy NG, Renz A, Mackenstedt U, Henkle-Dührsen K, de Bronsvoort MB, Tanya VN, Donnelly MJ, Trees AJ. 2000. Macrofilaricidal activity of tetracycline against the filarial nematode Onchocerca ochengi: elimination of Wolbachia precedes worm death and suggests a dependent relationship. Proc. R. Soc. B Biol. Sci. 267:1063-1069. http://dx.doi.org/10.1098/rspb.2000.1110.
19. Brouqui P, Fournier PE, Raoult D. 2001. Doxycycline and eradication of microfilaremia in patients with loiasis. Emerg. Infect. Dis. 7:604-605. http://dx.doi.org/10.3201/eid0707.017747.
20. Hoerauf A, Specht S, Buttner M, Pfarr K, Mand S, Fimmers R, Marfo-Debrekyei Y, Konadu P, Debrah AY, Bandi C, Brattig N, Albers A, Larbi J, Batsa L, Taylor MJ, Adjei O, Buttner DW. 2008. Wolbachia endobacteria depletion by doxycycline as antifilarial therapy has macrofilaricidal activity in onchocerciasis: a randomized placebo-controlled study. Med. Microbiol. Immunol. 197:295-311. http://dx.doi.org/10.1007/s00430-007-0062-1.
21. Hoerauf A, Specht S, Marfo-Debrekyei Y, Buttner M, Debrah AY, Mand S, Batsa L, Brattig N, Konadu P, Bandi C, Fimmers R, Adjei O, Buttner DW. 2009. Efficacy of 5-week doxycycline treatment on adult Onchocerca volvulus. Parasitol. Res. 104:437-447. http://dx.doi.org/10.1007/s00436-008-1217-8.
22. Wanji S, Tendongfor N, Nji T, Esum M, Che JN, Nkwescheu A, Alassa F, Kamnang G, Enyong PA, Taylor MJ, Hoerauf A, Taylor DW. 2009. Community-directed delivery of doxycycline for the treatment of onchocerciasis in areas of co-endemicity with loiasis in Cameroon. Parasit. Vectors 2:39. http://dx.doi.org/10.1186/1756-3305-2-39.
23. Taylor MJ, Hoerauf A, Townson S, Slatko BE, Ward SA. 18 July 2013. Anti-Wolbachia drug discovery and development: safe macrofilaricides for onchocerciasis and lymphatic filariasis. Parasitology http://dx.doi.org/10.1017/ S0031182013001108.
24. Hermans PG, Hart CA, Trees AJ. 2001. In vitro activity of antimicrobial agents against the endosymbiont Wolbachia pipientis. J. Antimicrob. Chemother. 47:659-663. http://dx.doi.org/10.1093/jac/47.5.659.
25. Fenollar F, Maurin M, Raoult D. 2003. Wolbachia pipientis growth kinetics and susceptibilities to 13 antibiotics determined by immunofluorescence staining and real-time PCR. Antimicrob. Agents Chemother. 47:1665-1671. http://dx.doi.org/10.1128/AAC.47.5.1665-1671.2003.
26. Townson S, Tagboto S, McGarry HF, Egerton GL, Taylor MJ. 2006. Onchocerca parasites and Wolbachia endosymbionts: evaluation of a spectrum of antibiotic types for activity against Onchocerca gutturosa in vitro. Filaria J. 5:4. http://dx.doi.org/10.1186/1475-2883-5-4.
27. Volkmann L, Fischer K, Taylor M, Hoerauf A. 2003. Antibiotic therapy in murine filariasis (Litomosoides sigmodontis): comparative effects of doxycycline and rifampicin on Wolbachia and filarial viability. Trop. Med. Int. Health 8:392-401. http://dx.doi.org/10.1046/j.1365-3156.2003.01040.x.
28. Townson S, Hutton D, Siemienska J, Hollick L, Scanlon T, Tagboto SK, Taylor MJ. 2000. Antibiotics and Wolbachia in filarial nematodes: antifilarial activity of rifampicin, oxytetracycline and chloramphenicol against Onchocerca gutturosa, Onchocerca lienalis and Brugia pahangi. Ann. Trop. Med. Parasitol. 94:801-816. http://dx.doi.org/10.1080/00034980020027988.
29. Richards FO, Jr, Amann J, Arana B, Punkosdy G, Klein R, Blanco C, Lopez B, Mendoza C, Dominguez A, Guarner J, Maguire JH, Eberhard M. 2007. No depletion of Wolbachia from Onchocerca volvulus after a short course of rifampin and/or azithromycin. Am. J. Trop. Med. Hyg. 77:878-882.
30. Specht S, Mand S, Marfo-Debrekyei Y, Debrah AY, Konadu P, Adjei O, Buttner DW, Hoerauf A. 2008. Efficacy of 2-and 4-week rifampicin treatment on the Wolbachia of Onchocerca volvulus. Parasitol. Res. 103: 1303-1309. http://dx.doi.org/10.1007/s00436-008-1133-y.
31. Morales-Hojas R, Cheke RA, Post RJ. 2006. Molecular systematics of five Onchocerca species (Nematoda: Filarioidea) including the human parasite, O. volvulus, suggest sympatric speciation. J. Helminthol. 80:281-290. http://dx.doi.org/10.1079/JOH2006331.
32. Renz A, Trees AJ, Achukwi D, Edwards G, Wahl G. 1995. Evaluation of suramin, ivermectin and CGP 20376 in a new macrofilaricidal drug screen, Onchocerca ochengi in African cattle. Trop. Med. Parasitol. 46:31-37.
33. Bronsvoort BM, Renz A, Tchakouté V, Tanya VN, Ekale DD, Trees AJ. 2005. Repeated high doses of avermectins cause prolonged sterilisation, but do not kill Onchocerca ochengi adult worms in African cattle. Filaria J. 4:8. http://dx.doi.org/10.1186/1475-2883-4-8.
34. Trees AJ, Wahl G, Klager S, Renz A. 1992. Age-related differences in parasitosis may indicate acquired immunity against microfilariae in cattle naturally infected with Onchocerca ochengi. Parasitology 104:247-252. http://dx.doi.org/10.1017/S0031182000061680.
35. Hansen RD, Trees AJ, Bah GS, Hetzel U, Martin C, Bain O, Tanya VN, Makepeace BL. 2011. A worm's best friend: recruitment of neutrophils by Wolbachia confounds eosinophil degranulation against the filarial nematode Onchocerca ochengi. Proc. R. Soc. B Biol. Sci. 278:2293-2302. http://dx.doi.org/10.1098/rspb.2010.2367.
36. Gilbert J, Nfon CK, Makepeace BL, Njongmeta LM, Hastings IM, Pfarr KM, Renz A, Tanya VN, Trees AJ. 2005. Antibiotic chemotherapy of onchocerciasis: in a bovine model, killing of adult parasites requires a sustained depletion of endosymbiotic bacteria (Wolbachia species). J. Infect. Dis. 192:1483-1493. http://dx.doi.org/10.1086/462426.
37. Srivastava A, Waterhouse D, Ardrey A, Ward SA. 2012. Quantification of rifampicin in human plasma and cerebrospinal fluid by a highly sensitive and rapid liquid chromatographic-tandem mass spectrometric method. J. Pharm. Biomed. Anal. 70:523-528. http://dx.doi.org/10.1016/j.jpba.2012.05.028.
38. Debrah AY, Mand S, Marfo-Debrekyei Y, Batsa L, Albers A, Specht S, Klarmann U, Pfarr K, Adjei O, Hoerauf A. 2011. Macrofilaricidal activity in Wuchereria bancrofti after 2 weeks treatment with a combination of rifampicin plus doxycycline. J. Parasitol. Res. 2011:201617. http://dx.doi.org/10.1155/ 2011/201617.
39. Gross DJ, Dellinger RP. 1988. Red/orange person syndrome. Cutis 42: 175-177.
40. Ali J, Ali N, Sultana Y, Baboota S, Faiyaz S. 2007. Development and validation of a stability-indicating HPTLC method for analysis of antitubercular drugs. Acta Chromatogr. 18:168-179.
41. Davey LA, Ferber MT, Kaye B. 1985. Comparison of the serum pharmacokinetics of a long acting and a conventional oxytetracycline injection. Vet. Rec. 117:426-429. http://dx.doi.org/10.1136/vr.117.17.426.
42. Nfon CK, Makepeace BL, Njongmeta LM, Tanya VN, Trees AJ. 2007. Lack of resistance after re-exposure of cattle cured of Onchocerca ochengi infection with oxytetracycline. Am. J. Trop. Med. Hyg. 76:67-72.
43. Diacon AH, Patientia RF, Venter A, van Helden PD, Smith PJ, McIlleron H, Maritz JS, Donald PR. 2007. Early bactericidal activity of highdose rifampin in patients with pulmonary tuberculosis evidenced by positive sputum smears. Antimicrob. Agents Chemother. 51:2994-2996. http://dx.doi.org/10.1128/AAC.01474- 06.
44. Watt G, Kantipong P, Jongsakul K, Watcharapichat P, Phulsuksombati D, Strickman D. 2000. Doxycycline and rifampicin for mild scrub-typhus infections in northern Thailand: a randomised trial. Lancet 356:1057-1061. http://dx.doi.org/10.1016/S0140-6736(00)02728-8.
45. Garraffo A, Dellamonica P, Fournier JP, Lapalus P, Bernard E. 1988. The effect of rifampicin on the pharmacokinetics of doxycycline. Infection 16:297-298. http://dx.doi.org/10.1007/BF01645076.
46. Colmenero JD, Fernandez-Gallardo LC, Agundez JA, Sedeno J, Benitez J, Valverde E. 1994. Possible implications of doxycycline-rifampin interaction for treatment of brucellosis. Antimicrob. Agents Chemother. 38: 2798-2802. http://dx.doi.org/10.1128/AAC.38.12.2798.
47. Aristoff PA, Garcia GA, Kirchhoff PD, Hollis Showalter HD. 2010. Rifamycins-obstacles and opportunities. Tuberculosis (Edinb.) 90:94-118. http://dx.doi.org/10.1016/j.tube.2010.02.001.
48. Schiefer A, Schmitz A, Schaberle TF, Specht S, Lammer C, Johnston KL, Vassylyev DG, Konig GM, Hoerauf A, Pfarr K. 2012. Corallopyronin A specifically targets and depletes essential obligate Wolbachia endobacteria from filarial nematodes in vivo. J. Infect. Dis. 206:249-257. http://dx.doi.org/10.1093/ infdis/jis341.
49. Rentsch A, Kalesse M. 2012. The total synthesis of corallopyronin A and myxopyronin B. Angew. Chem. Int. Ed. Engl. 51:11381-11384. http://dx.doi.org/10. 1002/anie.201206560.
50. Schaberle TF, Schiefer A, Schmitz A, Konig GM, Hoerauf A, Pfarr K. 2013. Corallopyronin A-a promising antibiotic for treatment of filariasis. Int. J. Med. Microbiol. http://dx.doi.org/10.1016/j.ijmm.2013.08.010.