Review on Pre-clinical Antimicrobial Assay
Keywords:
Animal models, Antimicrobial Assay, Artemia, Galleria mellonella, Hydractinia, waxmothAbstract
Pre-clinical antimicrobial testing is one costly step in antimicrobial drugs developoment. Costly effective methods in performing the in vitro and in vivo assay as part of pre-clinical stage is critical. We reviewed the current development of this stage. We found that standardization of agar diffusion techniques and measurement of minimal inhibitory concentrations in broth dilution methods serve as the primary reference for in vitro antimicrobial testing. In vivo, moral issues, ethics, costs, and the correlation of using animal models with human physiological conditions enforce us to seek alternative systems or animal models. Organ-on-a-Chip (OC) emerges as an ethically sound alternative system, yet in terms of cost and simulation of physiological conditions, there is still much progress to be made. Fruit fly (Drosophila melanogaster) and waxmoth (Galleria mellonella) are currently the main alternative animal models that are more affordable, simple, and ethically sound compared to worms, silkworms, mice, and primates. Artemia spp. and Hydractinia spp. have the potential to become new alternative animal models in simulating microbial infections and the efficacies of the antimicrobial that fight against it in the future
References
al-Bukhari, M. b. (846). Al-Jami al-Musnad as-Sahih al-Mukhtasar min Umur Rasulilah ﷺ wa Sunanihi wa Ayyamihi. Bukhara.
Asai, M., Li, Y., Newton, S. M., Robertson, B. D., & Langford, P. R. (2023). Galleria mellonella-Intracellular Bacteria Pathogen Infection Models: the Ins and Outs. FEMS Microbiol. Rev., 47(2), 011. https://doi.org/10.1093/femsre/fuad011
Baruah, K., Phong, H. P., Norouzitallab, P., Defoirdt, T., & Bossier, P. (2015). The Gnotobiotic Brine Shrimp (Artemia franciscana) Model System Reveals that the Phenolic Compound Pyrogallol Protects Against Infection Through its Prooxidant Activity. Free Radicals Biol. Med., 89, 593-601. https://doi.org/10.1016/j.freeradbiomed.2015.10.397
Birch, J. (2020). The place of animals in Kantian ethics. Biology & Philosophy, 35, 252. https://doi.org/10.1007/s10539-019-9712-0
Cathriona, M. R., Kanska, J., Duffy, D. J., Seoighe, C., Cunningham, S., Plickert, G., & Frank, U. (2011). Induced stem cell neoplasia in a cnidarian by ectopic expression of a POU domain transcription factor. Development, 138(12), 2429-2439. https://doi.org/10.1242/dev.064931
Cheluvappa, R., Scowen, P., & Eri, R. (2017). Ethics of animal research in human disease remediation, its institutional teaching, and alternatives to animal. Pharmacol. Res. Perspect., 5(4), e00332. https://doi.org/10.1002/prp2.332
Chicu, S. A. (2019). Structure–activity relationship (SAR) study of some aliphatic and aromatics carboxyl– and α–amino–C–phosphonates congeneric esters and Schiff derivatives using a developed Köln–model (Hydractinia echinata Toxicity Screening Test System. VI.). Comput. Toxicol., 12, 100099. https://doi.org/10.1016/j.comtox.2019.100099
Chicu, S. A., Schannen, L., Putz, M. V., & Simu, G.-M. (2016). Hydractinia echinata test-system.IV. Toxis synergism of human pharmaceuticals in mixture with iodoform. Ecotoxicol. Environ. Saf., 134(1), 80-85. https://doi.org/10.1016/j.ecoenv.2016.08.014
Colgan, R. (2010). Advice to the Young Physician: On the Art of Medicine. New York: Springer Science.
Cusack, T., Ashley, E., Ling, C., Roberts, T., Turner, P., Wangrangsimakul, T., & Dance, D. (2019). Time to switch from CLSI to EUCAST? A southeast asian perspective. Clin. Microbiol. Infect., 25(7), 782-785. https://doi.org/10.1016/j.cmi.2019.03.016
Davis, M. M., Alvarez, F. J., Ryman, K., Holm, A. A., Ljungdahl, P. O., & Engstorm, Y. (2011). Wild-type Drosophila melanogaster as a model host to analyze nitrogen source dependent virulence of Candida albicans. PloS One, 6(11), e27434. https://doi.org/10.1371/journal.pone.0027434
Dionne, M. S., Ghori, N., & Schneider, D. S. (2003). Drosophila melanogaster is a genetically tractable model host for Mycobacterium marinum. Infect. Immun., 71(6), 3540-3550. https://doi.org/10.1128/iai.71.6.3540-3550.2003
Dzutsev, A., Badger, J. H., Perez-Chanona, E., Roy, S., Salcedo, R., Smith, C. K., & Trinchieri, G. (2017). Microbes and Cancer. Annu. Rev. Immun., 35, 199-228. https://doi.org/10.1146/annurev-immunol-051116-052133
Eloff, J. N. (2019). Avoiding pitfalls in determining antimicrobial activity of plant extracts and publishing the results. BMC Complementary Altern. Med., 19, 106-114. https://doi.org/10.1186/s12906-019-2519-3
Freires, I. A., Sardi, J. d., de Castro, R. D., & Rosalen, P. L. (2017). Alternative Animal and Non-Animal Models for Drug Discovery and Development: Bonus or Burden. Pharm. Res., 34, 681-686. https://doi.org/10.1007/s11095-016-2069-z
Galloway-Pena, J., Iliev, I. D., & McAllister, F. (2024). Fungi in cancer. Nat. Rev. Cancer, 24, 295-298. https://doi.org/10.1038/s41568-024-00665-y
GBD 2019 Antimicrobial Resistance Collaborators. (2022). Global mortality associated with 33 bacterial pathogens in 2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet, 400, 2221-2248. https://doi.org/10.1016/S0140-6736(22)02185-7
Grassart, A., Malarde, V., Gobaa, S., Sartori-Rupp, A., Kerns, J., Karalis, K., . . . Sauvonnet, N. (2019). Bioengineered Human Organ-on-a-Chip Reveals Intestinal Microenvironment and Mechanical Forces Impacting Shigella Infection. Cell Host & Microbe, 26, 435-444. https://doi.org/10.1016/j.chom.2019.08.007
Guo, H., Rischer, M., Sperfeld, M., Weigel, C., Menzel, K. D., Clardy, J., & Beemelmanns, C. (2017). Natural products and morphogenic activity of γ-Proteobacteria associated with the marine hydroid polyp Hydractinia echinata. Bioorg. Med. Chem., 25(22), 6088-6097. https://doi.org/10.1016/j.bmc.2017.06.053
Guo, H., Rischer, M., Wastermann, M., & Beemelmanns, C. (2021). Two Distinct Bacterial Biofilm Components Trigger Metamorphosis in the Colonial Hydrozoan Hydractinia echinata. MBio, 12(3), 10-1128. https://doi.org/10.1128/mbio.00401-21
Hala, S., Malaikah, M., Huang, J., Bahitham, W., Fallatah, O., Zakri, S., . . . Pain, A. (2024). The emergence of highly resistant and hypervirulent Klebsiella pneumoniae CC14 clone in a tertiary hospital over 8 years. Genome Med., 16, 58. https://doi.org/10.1186/s13073-024-01332-5
Hanbal, A. b. (842). Musnad Ahmad. Baghdad.
Hewitt, W., & Vincent, S. (1989). Theory and Application of Microbiological Assay. London: Academic Press Inc.
Jalili-Firoozinezhad, S., Gazzaniga, F. S., Calamari, E. L., Camacho, D. M., Fadel, C. W., Bein, A., . . . Ingber, D. E. (2019). A complex human gut microbiome cultured in an anaerobic intestine-on-a-chip. Nat. Biomed. Eng., 3, 520-531. https://doi.org/10.1038/s41551-019-0397-0
Jalili-Firoozinezhad, S., Miranda, C. C., & Cabral, J. M. (2021). Modeling Human Body on Microfluidic Chips. Trends Biotech., 39(8), 838-852. https://doi.org/10.1016/ j.tibtech.2021.01.004
Jang, K.-J., Otieno, M. A., Ronxhi, J., Lim, H.-K., Ewart, L., Kodella, K., . . . Hamilton, G. (2019). Reproducing human and cross-species drug toxicities using a Liver-Chip. Sci. Transl. Med., 11(517), eaax5516. https://doi.org/10.1126/scitranslmed.aax5516
Jensen, H. E. (2020). Animal Models of Invasive Mycoses. J. Pathol. Microbiol. Immun., 130, 427-435. https://doi.org/10.1111/apm.13110
Kaito, C., Murakami, K., & Furuta, K. (2020). Animal infection models using non-mammals. Microbiol. Immun., 64(9), 585-592. https://doi.org/10.1111/1348-0421.12834
Kim, D. H., & Flavell, S. W. (2020). Host-microbe interactions and the behavior of Caenorhabditis elegans. J. Neurogenet., 34(3), 500-509. https://doi.org/10.1080/01677063.2020.1802724
Klancnik, A., Piskernik, S., Jersek, B., & Mozina, S. S. (2010). Evaluation of diffusion and dilution methods to determine the antibacterial activity. J. Microbiol. Methods, 81, 121-126. https://doi.org/10.1016/j.mimet.2010.02.004
Lall, N., Henley-Smith, C., De Canha, M. N., Oosthuizen, C. B., & Berrington, D. (2013). Viability Reagent, PrestoBlue, in Comparison with Other Available Reagents, Utilized in Cytotoxicity and Antimicrobial Assays. Int. J. Microbiol., 2013(1), 420601. https://doi.org/10.1155/2013/420601
Lee, M.-N., Kim, S.-K., Li, X.-H., & Lee, J.-H. (2014). Bacterial virulence analysis using brine shrimp as an infection model in relation to the importance of quorum sensing and proteases. J. Gen. Appl. Microbiol., 60(5), 169-174. https://doi.org/10.2323/jgam.60.169
Libralato, G., Prato, E., Migliore, L., Cicero, A., & Manfra, L. (2016). A review of toxicity testing protocols and endpoints with Artemia spp. Ecol. Indic., 69, 35-49. https://doi.org/10.1016/j.ecolind.2016.04.017
Liegeois, S., & Ferrandon, D. (2022). Sensing microbial infections in the Drosophila melanogaster genetic model organism. Immunogenetics, 74, 35-62. https://doi.org/10.1007/s00251-021-01239-0
Liu, Y.-Y., Wang, Y., Walsh, T. R., Yi, L.-X., Zhang, R., Spencer, J., . . . Shen, J. (2016). Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect. Dis., 16(2), 161-168. https://doi.org/10.1016/S1473-3099(15)00424-7
Mansfield, B. E., Dionne, M. S., Schneider, D. S., & Freitag, N. E. (2003). Exploration of host–pathogen interactions using Listeria monocytogenes and Drosophila melanogaster. Cell. Microbiol., 5(12), 901-911. https://doi.org/10.1046/j.1462-5822.2003.00329.x
Moradi, E., Jalili-Firoozinezhad, S., & Solati-Hashjin, M. (2020). Microfluidic organ-on-a-chip model of human liver tissue. Acta Biomater., 116, 67-83. https://doi.org/10.1016/j.actbio.2020.08.041
Morton, D., Dunphy, G., & Chadwick, J. (1987). Reactions of hemocytes of immune and non-immune Galleria mellonella larvae to Proteusmirabilis. Dev. Comp. Immunol., 11(1), 47-55. https://doi.org/10.1016/0145-305X(87)90007-3
Mulchandani, R., Wang, Y., Gilbert, M., & Van Boeckel, T. P. (2023). Global trends in antimicrobial use in foodproducing animals: 2020-2030. PLoS Global Public Health, 3(2), e00001305. https://doi.org/10.1371/journal.pgph.0001305
Muslim, B. A.-H. (875). Shahih Muslim. Naysaburi.
Nikolaev, M., Mitrofanova, O., Broguiere, N., Geraldo, S., Dutta, D., Tabata, Y., . . . Lutolf, M. P. (2020). Homeostatic mini-intestines through scaffold-guided organoid morphogenesis. Nature, 585, 574-578. https://doi.org/10.1038/s41586-020-2724-8
Raharjo, H. (2021). Serangan Hama Ngengat Lilin pada Koloni Lebah Madu (Apis cerana) di Hutan Pendidikan Wanagama I. DIY: Skripsi S1 Kehutanan UGM.
Robinson, B. N., Krieger, K., Khan, F. M., Huffman, W., Chang, M., Naik, A., . . . Gaudino, M. (2019). The current state of animal models in research: A review. Int. J. Surg., 72, 9-13. https://doi.org/10.1016/j.ijsu.2019.10.015
Roy, S., Baruah, K., Bossier, P., Vanrompay, D., & Norouzitallab, P. (2022). Induction of transgenerational innate immune memory against Vibrio infections in a brine shrimp (Artemia franciscana) model. Aquaculture, 557, 738309. https://doi.org/10.1016/j.aquaculture.2022.738309
Schar, D., Zhao, C., Wang, Y., Larsson, J., Gilbert, M., & Van Boeckel, T. P. (2021). Twenty-year trends in antimicrobial resistance from aquaculture and fisheries in Asia. Nat. Commun., 12, 5384-5394. https://doi.org/10.1038/s41467-021-25655-8
Singh, A. K., & Gupta, U. D. (2018). Animal models of tuberculosis: Lesson learnt. Indian J. Med. Res., 147, 456-463. https://doi.org/10.4103/ijmr.IJMR_554_18
Thacker, V. V., Dhar, N., Sharma, K., Barrile, R., Karalis, K., & McKinney, J. D. (2020). A lung on a chip model of early Mycobacterium tuberculosis infection reveals an essential role for alveolar epithelial cells in controlling bacterial growth. eLife, 2020, e59961. https://doi.org/10.7554/eLife.59961
Toure, H., Herrmann, J.-L., Szuplewski, S., & Girard-Misguich, F. (2023). Drosophila melanogaster as an organism model for studying cystic fibrosis and its major associated microbial infections. Infect. Immun., 91, e00240-23. https://doi.org/10.1128/iai.00240-23
Van Norman, G. A. (2019). Limitations of Animal Studies for Predicting Toxicity in Clinical Trials. J. Am. Coll. Cardiol.: Basic Transl. Sci., 4(7), 845-854. https://doi.org/10.1016%2Fj.jacbts.2019.10.008
Van Norman, G. A. (2020). Limitations of Animal Studies for Predicting Toxicity in Clinical Trials Part 2. J. Am. Coll. Cardiol.: Basic Transl. Sci., 5(4), 387-397. https://doi.org/10.1016%2Fj.jacbts.2020.03.010
Vindri, R. (2018). Pengaruh Modifikasi Pakan Formula terhadap Biologi Ngengat Lilin Galleria mellonella (L.) (Lepidoptera: Pyralidae). Bogor: Skripsi S1 Proteksi Tanaman IPB University.
Vogelsang, T. (1963). A serious sentence passed against the discoverer of the leprosy Bacillus (Gerhard Armauer Hansen), in 1880. Med. Hist., 7(2), 182-186. https://doi.org/10.1017/S0025727300028210
WHO. (2020). The Top 10 Causes of Death. Retrieved 05 28, 2024, from https://www.who.int/news-room/fact-sheets/detail/the-top-10-causes-of-death
WHO. (2023). Antimicrobial Resistance. Retrieved 06 06, 2024, from https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance
Yuan, L., Gordesky-Gold, B., Leney-Greene, M., Weinbren, N. L., Tudor, M., & Cherry, S. (2018). Inflammation-induced, STING-dependent autophagy restricts Zika virus infection in the Drosophila brain. Cell Host & Microbe, 24(1), 57-68. https://doi.org/10.1016/j.chom.2018.05.022
Zak, O., O'Reilly, T., & . (1991). Animal Models in the Evaluation of Antimicrobial Agents. Antimicrob. Agents Chemother., 35(8), 1527-1531. https://doi.org/10.1128%2Faac.35.8.1527
Zarate-Potes, A., Ocampo, I. D., & Cadavid, L. F. (2019). The putative immune recognition repertoire of the model cnidarian Hydractinia symbiolongicarpus is large and diverse. Gene, 684, 104-117. https://doi.org/10.1016/j.gene.2018.10.068
Zhang, Y., Wang, D., Zhang, Z., Wang, Z., Zhang, D., & Yin, H. (2018). Transcriptome analysis of Artemia sinica in response to Micrococcus lysodeikticus infection. Fish Shellfish Immunol., 81, 92-98. https://doi.org/10.1016/j.fsi.2018.06.033
Zheng, L.-P., Hou, L., Chang, A. K., Yu, M., Ma, J., Li, X., & Zou, X.-Y. (2011). Expression Pattern of A Gram-negative bacteria-binding protein in early embryonic development of Artemia sinica and after bacterial challenge. Dev. Comp. Immunol., 35(1), 35-43. https://doi.org/10.1016/j.dci.2010.08.002
