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In Vitro and in Vivo Trypanocidal Efficacy of Synthesized Nitrofurantoin Analogs

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In Vitro and in Vivo Trypanocidal Efficacy of Synthesized Nitrofurantoin Analogs molecules Article In Vitro and In Vivo Trypanocidal Efficacy of Synthesized Nitrofurantoin Analogs Linous Munsimbwe 1, Anna Seetsi 2 , Boniface Namangala 3, David D. N’Da 4, Noboru Inoue 5 and Keisuke Suganuma 6,* 1 Ministry of Fisheries and Livestock, Department of Veterinary Services, Mulungushi House, P.O. Box 50600, Ridgeway, Lusaka 15100, Zambia; [email protected] 2 Unit for Environmental Science and Management, Faculty of Natural and Agricultural Sciences, North-West University, Potchefstroom 2531, South Africa; [email protected] 3 Department of Paraclinical Studies, School of Veterinary Medicine, University of Zambia, P.O. Box 32379, Lusaka 10101, Zambia; [email protected] 4 Centre of Excellence for Pharmaceutical Sciences (PHARMACEN), North-West University, Potchefstroom 2520, South Africa; [email protected] 5 OIE Reference Laboratory for Surra, National Research Centre for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080-8555, Japan; [email protected] 6 Research Center for Global Agromedicine, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080-8555, Japan * Correspondence: [email protected]; Tel.: +81-155-49-5697 Abstract: African trypanosomes cause diseases in humans and livestock. Human African trypanoso- miasis is caused by Trypanosoma brucei rhodesiense and T. b. gambiense. Animal trypanosomoses have major effects on livestock production and the economy in developing countries, with disease Citation: Munsimbwe, L.; Seetsi, A.; management depending mainly on chemotherapy. Moreover, only few drugs are available and these Namangala, B.; N’Da, D.D.; Inoue, N.; have adverse effects on patients, are costly, show poor accessibility, and parasites develop drug Suganuma, K. In Vitro and In Vivo resistance to them. Therefore, novel trypanocidal drugs are urgently needed. Here, the effects of Trypanocidal Efficacy of Synthesized synthesized nitrofurantoin analogs were evaluated against six species/strains of animal and human Nitrofurantoin Analogs. Molecules 2021, 26, 3372. https://doi.org/ trypanosomes, and the treatment efficacy of the selected compounds was assessed in vivo. Analogs 10.3390/molecules26113372 11 and 12, containing 11- and 12-carbon aliphatic chains, respectively, showed the highest trypanoci- dal activity (IC50 < 0.34 µM) and the lowest cytotoxicity (IC50 > 246.02 µM) in vitro. Structure-activity Academic Editors: Paula A. C. Gomes relationship analysis suggested that the trypanocidal activity and cytotoxicity were related to the and Diego Muñoz-Torrero number of carbons in the aliphatic chain and electronegativity. In vivo experiments, involving oral treatment with nitrofurantoin, showed partial efficacy, whereas the selected analogs showed no treat- Received: 26 April 2021 ment efficacy. These results indicate that nitrofurantoin analogs with high hydrophilicity are required Accepted: 25 May 2021 for in vivo assessment to determine if they are promising leads for developing trypanocidal drugs. Published: 2 June 2021 Keywords: animal trypanosomosis; human African trypanosomiasis; nitrofurantoin analog; try- Publisher’s Note: MDPI stays neutral panocidal drug with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Introduction African trypanosomes, transmitted by tsetse fly, cause several diseases in both humans and livestock on the Sub-Saharan African continent. Human African trypanosomiasis Copyright: © 2021 by the authors. (HAT) is caused by Trypanosoma brucei gambiense and T. b. rhodesiense. The disease has Licensee MDPI, Basel, Switzerland. devastating socio-economic impacts, such as reduced income generation, negative effects on This article is an open access article distributed under the terms and the education of children, increased healthcare costs, and long-term health consequences [1, conditions of the Creative Commons 2]. In contrast, animal African trypanosomosis, which is caused by T. congolense, T. vivax, Attribution (CC BY) license (https:// and T. brucei brucei, represents a major health concern in animal development, and its creativecommons.org/licenses/by/ deleterious impacts can be manifested in terms of reduced livestock productivity, costly 4.0/). disease control, and trade implications, as well as negative impacts on agriculture and Molecules 2021, 26, 3372. https://doi.org/10.3390/molecules26113372 https://www.mdpi.com/journal/molecules Molecules 2021, 26, x FOR PEER REVIEW 2 of 11 Molecules 2021,, 26,, xx FORFOR PEER REVIEW 2 of 11 ment, and its deleterious impacts can be manifested in terms of reduced livestock produc- ment, and its deleterious impacts can be manifested in terms of reduced livestock produc- Molecules 2021, 26, 3372 tivity, costly disease control, and trade implications, as well as negative impacts on2 of agri- 11 tivity, costly disease control, and trade implications, as well as negative impacts on agri- culture and food security [3,4]. Surra is an animal trypanosomosis caused by T. evansi in- culture and food security [3,4]. Surra is an animal trypanosomosis caused by T. evansi in- fection. It is mechanically transmitted by hematophagous biting flies such as Tabanus spp., fection. It is mechanically transmitted by hematophagous biting flies such as Tabanus spp., Stomoxys spp., and species of tsetse flies [5]. Animal trypanosomoses (AT), including ani- foodStomoxys security spp., [3,4 and]. Surra species is an of animal tsetse flies trypanosomosis [5]. Animal trypanosomoses caused by T. evansi (AT),infection. including It isani- mal African trypanosomosis and surra, are economically important diseases in animals. mechanicallymal African transmittedtrypanosomosis by hematophagous and surra, are economically biting flies such important as Tabanus diseasesspp., Stomoxysin animals. They cause high mortality, low milk and meat production, poor carcass quality, reduced spp.,They and cause species high of mortality, tsetse flies low [5]. milk Animal and trypanosomoses meat production, (AT), poor including carcass animalquality, African reduced reproductive performance, and decreased draught animal power and manure production, trypanosomosisreproductive performance, and surra, are and economically decreased draught important animal diseases power in and animals. manure They production, cause as well as immunosuppression in livestock [3,5]. highas well mortality, as immunosuppression low milk and meat in production, livestock [3,5]. poor carcass quality, reduced reproductive HAT/AT control requires an integrated approach involving the use of trypanocidal performance,HAT/AT and control decreased requires draught an integrated animal power approach and involving manure production, the use of trypanocidal as well as drugs [3,6], reduction in the number of vectors, and low contact between hosts and vectors immunosuppressiondrugs [3,6], reduction in livestockin the number [3,5]. of vectors, and low contact between hosts and vectors [7]. Owing to the challenges in vector control programs and vaccine development, [7].HAT/AT Owing to control the challenges requires an in integrated vector control approach programs involving and thevaccine use of development, trypanoci- HAT/AT control primarily depends on chemotherapy using anti-parasitic agents. Cur- dalHAT/AT drugs [ 3control,6], reduction primarily in the depends number on of chemotherapy vectors, and lowusing contact anti-parasitic between agents. hosts and Cur- rently, the nifurtimox–eflornithine combination therapy (NECT) and fexinidazole are ap- vectorsrently, [ 7the]. Owingnifurtimox to the–eflornithine challenges combination in vector control therapy programs (NECT) and fexinidazole vaccine develop- are ap- proved for treating HAT caused by T. b. gambiense [8]. Particularly, fexinidazole was the ment,proved HAT/AT for treating control HAT primarily caused depends by T. b. gambiense on chemotherapy [8]. Particularly, using anti-parasitic fexinidazole agents. was the first oral drug approved for HAT treatment, which shows satisfactory treatment efficacy Currently,first oral thedrug nifurtimox–eflornithine approved for HAT treatment, combination which therapy shows (NECT) satisfactory and fexinidazoletreatment efficacy are against second-stage HAT, as compared to the nifurtimox–eflornithine combination ther- approvedagainst second for treating-stageHAT HAT caused, as compared by T. b. to gambiense the nifurtimox[8]. Particularly,–eflornithine fexinidazole combination was ther- apy [9]. In contrast, no orally administered and safe drugs are available against HAT theapy first [9] oral. In drugcontrast, approved no orally for HAT administered treatment, and which safe shows drugs satisfactory are available treatment against effi-HAT caused by T. b. rhodesiense and AT. Therefore, the screening and development of safe and cacycaused against by T. second-stage b. rhodesiense HAT, and asAT. compared Therefore, to the screening nifurtimox–eflornithine and development combination of safe and effective compounds for treating HAT/AT are urgently required. therapyeffective [9]. compounds In contrast, for no treating orally administered HAT/AT are and urgently safe drugs required. are available against HAT Nitrofurantoin is a hypoxic agent with activity against a myriad of anaerobic patho- causedNitrofurantoin by T. b. rhodesiense is a hypoxicand AT. Therefore,agent with theactivity screening against and a myriad development of anaerobic of safe patho- and gens. This nitrofuran compound contains a Schiff
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