Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-18T15:41:39.763Z Has data issue: false hasContentIssue false

Modelling appropriate use of trypanocides to restrict wide-spread multi-drug resistance during chemotherapy of animal African trypanosomiasis

Published online by Cambridge University Press:  20 December 2018

Ibrahim I. Wangwe
Affiliation:
Centre for Biotechnology and Bioinformatics, University of Nairobi, P.O. Box 30197, Nairobi, Kenya International Centre of Insect Physiology and Ecology, P.O. Box 30772, Nairobi, Kenya
Sarah A. Wamwenje
Affiliation:
Centre for Biotechnology and Bioinformatics, University of Nairobi, P.O. Box 30197, Nairobi, Kenya International Centre of Insect Physiology and Ecology, P.O. Box 30772, Nairobi, Kenya
Caroline Mirieri
Affiliation:
Kiboko Zoological Investigations and Efficacy Trials Centre, P.O. Box 21, Kiboko, Makindu, Kenya
Nicodemus M. Masila
Affiliation:
Kenya Tsetse and Trypanosomiasis Eradication Council (KENTTEC), P.O. Box 106-80403, Kwale, Kenya
Lillian Wambua
Affiliation:
International Centre of Insect Physiology and Ecology, P.O. Box 30772, Nairobi, Kenya School of Biological Sciences, University of Nairobi, P.O. Box 30197, Nairobi, Kenya
Benard W. Kulohoma*
Affiliation:
Centre for Biotechnology and Bioinformatics, University of Nairobi, P.O. Box 30197, Nairobi, Kenya International Centre of Insect Physiology and Ecology, P.O. Box 30772, Nairobi, Kenya
*
Author for correspondence: Benard W. Kulohoma, E-mail: bkulohoma@uonbi.ac.ke

Abstract

Trypanocide resistance remains a huge challenge in the management of animal African trypanosomiasis. Paucity of data on the prevalence of multi-drug resistant trypanosomes has greatly hindered optimal veterinary management practices. We use mathematical model predictions to highlight appropriate drug regimens that impede trypanocide resistance development in cattle. We demonstrate that using drugs in decreasing resistance order results in a negligible increase in number of cattle with resistant infection, in contrast to a more pronounced increase from trypanocide use in increasing resistance order. We demonstrate that the lowest levels of trypanocide resistance are achieved with combination therapy. We also show that increasing the number of cattle treated leads to a progressive reduction in the number of cattle with drug resistant infections for treatments of up to 80% of the cattle population for the combination treatment strategy. Our findings provide an initial evidence-based framework on some essential practices that promote optimal use of the handful of trypanocides. We anticipate that our modest forecasts will improve therapeutic outcomes by appropriately informing on the best choice, and combination of drugs that minimize treatment failure rates.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alingu, RA, Muhanguzi, D, MacLeod, E, Waiswa, C and Fyfe, J (2014) Bovine trypanosome species prevalence and farmers' trypanosomiasis control methods in south-western Uganda. Journal of the South African Veterinary Association 85, 1094.Google Scholar
Brun, R and Balmer, O (2006) New developments in human African trypanosomiasis. Current Opinion in Infectious Diseases 19, 415420.Google Scholar
Delespaux, V, Geysen, D, Van den Bossche, P and Geerts, S (2008) Molecular tools for the rapid detection of drug resistance in animal trypanosomes. Trends in Parasitology 24, 236242.Google Scholar
FAO (1987) 27 – Chemotherapy against African animal trypanosomiasis: Its strengths and limitations. Livestock production in tsetse affected areas of Africa, Proceedings of a meeting held in Nairobi, Kenya from the 23rd to 27th November 1978. Available at http://www.fao.org/wairdocs/ILRI/x5443E/x5443e5440u.htm.Google Scholar
FAO (1992) Chapter 5: Distribution of Glossina. Tsetse biology, systematics and distribution; techniques. Available at http://www.fao.org/docrep/009/p5178e/p5178e00.htm.Google Scholar
FAO (1998 a) Chapter 4: Control. A field guide for the diagnosis, treatment and prevention of African animal trypanosomosis. Available at http://www.fao.org/tempref/docrep/fao/006/x0413e/x0413e04.pdf – [0,{%22name%22:%22Fit%22}], 6–7.Google Scholar
FAO (1998 b) Current situation of resistance against trypanocidal drugs. Drug management and parasite resistance in bovine trypanosomiasis in Africa. Available at http://www.fao.org/docrep/003/w9791e/w9791e00.HTM.Google Scholar
Franco, JR, Simarro, PP, Diarra, A and Jannin, JG (2014) Epidemiology of human African trypanosomiasis. Clinical Epidemiology 6, 257275.Google Scholar
G7 2017 ITALIA (2017) Common approach of G7 CVOs on the definitions of therapeutic responsible and prudent use of antimicrobials in animals. G7 -CVOs Second Forum – AMR 2, 17. http://www.salute.gov.it/imgs/C_17_notizie_3118_listaFile_itemName_0_file.pdfGoogle Scholar
Geerts, S, Holmes, PH, Eisler, MC and Diall, O (2001) African bovine trypanosomiasis: the problem of drug resistance. Trends in Parasitology 17, 2528.Google Scholar
Giordani, F, Morrison, LJ, Rowan, TG, HP, DEK and Barrett, MP (2016) The animal trypanosomiases and their chemotherapy: a review. Parasitology 143, 18621889.Google Scholar
Holt, HR, Selby, R, Mumba, C, Napier, GB and Guitian, J (2016) Assessment of animal African trypanosomiasis (AAT) vulnerability in cattle-owning communities of sub-Saharan Africa. Parasites & Vectors 9, 53.Google Scholar
Kajita, E, Okano, JT, Bodine, EN, Layne, SP and Blower, S (2007) Modelling an outbreak of an emerging pathogen. Nature Reviews Microbiology 5, 700709.Google Scholar
KENTTEC (2017) Tsetse and Trypanosomiasis Problem in Kenya. Available at http://www.kenttec.go.ke/tsetse-and-trypanosomiasis-problem-in-kenya/ (Accessed 11 July 2018).Google Scholar
Kohanski, MA, Dwyer, DJ and Collins, JJ (2010) How antibiotics kill bacteria: from targets to networks. Nature Reviews Microbiology 8, 423435.Google Scholar
Kroubi, M, Karembe, H and Betbeder, D (2011) Drug delivery systems in the treatment of African trypanosomiasis infections. Expert Opinion on Drug Delivery 8, 735747.Google Scholar
Kuzoe, FA (1993) Current situation of African trypanosomiasis. Acta Tropica 54, 153162.Google Scholar
Laufer, MK, Takala-Harrison, S, Dzinjalamala, FK, Stine, OC, Taylor, TE and Plowe, CV (2010) Return of chloroquine-susceptible falciparum malaria in Malawi was a reexpansion of diverse susceptible parasites. Journal of Infectious Diseases 202, 801808.Google Scholar
Leak, SGA (1998) Tsetse Biology and Ecology: Their Role in the Epidemiology and Control of Trypanosomosis. Nairobi, Kenya: CABI Publishing and ILRI.Google Scholar
Lipsitch, M and Moxon, ER (1997) Virulence and transmissibility of pathogens: what is the relationship? Trends in Microbiology 5, 3137.Google Scholar
Maichomo, MW, Ndungu, JM, Ngare, PM and Ole-Mapenay, IM (2005) The performance of Orma Boran and Maasai Zebu crossbreeds in a trypanosomosis endemic area of Nguruman, south western Kenya. Onderstepoort Journal of Veterinary Research 72, 8793.Google Scholar
Mbahin, N, Affognon, H, Andoke, J, Tiberius, M, Mbuvi, D, Otieno, J and Muasa, P and Saini, RK (2013) Parasitological prevalence of bovine trypanosomiasis in Kubo division of Kwale county of coastal Kenya: baseline survey. American Journal of Animal and Veterinary Sciences 8, 2836.Google Scholar
Mdachi, RE, Murilla, GA, Omukuba, JN and Cagnolati, V (1995) Disposition of diminazene aceturate (Berenil) in trypanosome-infected pregnant and lactating cows. Veterinary Parasitology 58, 215225.Google Scholar
Melaku, A and Bekele, B (2013) Drugs and drug resistance in African animal trypanosomosis: a review. European Journal of Applied Sciences 5, 8491.Google Scholar
Moore, S, Shrestha, S, Tomlinson, KW and Vuong, H (2012) Predicting the effect of climate change on African trypanosomiasis: integrating epidemiology with parasite and vector biology. Journal of the Royal Society, Interface 9, 817830.Google Scholar
Muhanguzi, D, Picozzi, K, Hatendorf, J, Thrusfield, M, Welburn, SC, Kabasa, JD and Waiswa, C (2014) Improvements on restricted insecticide application protocol for control of human and animal African trypanosomiasis in eastern Uganda. PLoS Neglected Tropical Diseases 8, e3284.Google Scholar
Muraguri, GR, McLeod, A, McDermott, JJ and Taylor, N (2005) The incidence of calf morbidity and mortality due to vector-borne infections in smallholder dairy farms in Kwale District, Kenya. Veterinary Parasitology 130, 305315.Google Scholar
Murilla, GA, Mdachi, RE, Ismail, AA and Karanja, WM (1996) Bioavailability, pharmacokinetics, and tissue distribution of 14C homidium after parenteral administration to Boran cattle. Journal of Veterinary Pharmacology and Therapeutics 19, 142148.Google Scholar
Nosten, F and White, NJ (2007) Artemisinin-based combination treatment of falciparum malaria. The American Journal of Tropical Medicine and Hygiene 77(6 Suppl):181192.Google Scholar
Pepin, J (2007) Combination therapy for sleeping sickness: a wake-up call. Journal of Infectious Diseases 195, 311313.Google Scholar
Priotto, G, Kasparian, S, Ngouama, D, Ghorashian, S, Arnold, U, Ghabri, S and Karunakara, U (2007) Nifurtimox-eflornithine combination therapy for second-stage Trypanosoma brucei gambiense sleeping sickness: a randomized clinical trial in Congo. Journal of Biochemistry and Molecular Biology 45, 14351442.Google Scholar
Sum, A (2014) Body warns over tsetse flies threat. Standard Digital. Available at https://www.standardmedia.co.ke/article/2000104284/body-warns-over-tsetse-flies-threat.Google Scholar
Vaumourin, E, Vourc'h, G, Gasqui, P and Vayssier-Taussat, M (2015) The importance of multiparasitism: examining the consequences of co-infections for human and animal health. Parasites & Vectors 8, 545.Google Scholar
Weinberger, DM, Dagan, R, Givon-Lavi, N, Regev-Yochay, G, Malley, R and Lipsitch, M (2008) Epidemiologic evidence for serotype-specific acquired immunity to pneumococcal carriage. Journal of Infectious Diseases 197, 15111518.Google Scholar
Wenzler, T, Schumann Burkard, G, Schmidt, RS, Maser, P, Bergner, A, Roditi, I and Brun, R (2016) A new approach to chemotherapy: drug-induced differentiation kills African trypanosomes. Scientific Reports 6, 22451.Google Scholar
Supplementary material: File

Wangwe et al. supplementary material

Wangwe et al. supplementary material 1
Download Wangwe et al. supplementary material(File)
File 3.4 MB