Occurrence of Multi-Drug-Resistant Escherichia coli in Chickens, Humans, Rodents and Household Soil in Karatu, Northern Tanzania
Abstract
:1. Introduction
2. Results
2.1. Isolation of Escherichia coli from the Samples
2.2. Antibiotic Resistance of E. coli Isolates from Chickens, Humans, Rodents and Soil
2.3. Multidrug-Resistance (MDR) of Escherichia coli Isolates from All Samples
2.4. Prevalence of MDR Isolates of E. coli in Different Locations of Karatu
2.5. Phenotypic Patterns of MDR E. coli Isolates from Chickens, Humans, Rodents and Soil
3. Discussion
4. Materials and Methods
4.1. Study Location
4.2. Sampling Strategy
4.3. Trapping of Rodents for Sample Collection
4.4. Collection of Samples from Humans, Chickens and Soil
4.5. Culture, Isolation and Identification of E. coli Isolates
4.6. Antibiotic Susceptibility Testing of E. coli Isolates
4.7. Statistical Analyses
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Islam, M.; Nayeem, M.; Hasan, M.; Sobur, M.; Ievy, S.; Rahman, S.; Kafi, M.; Ashour, H.M.; Rahman, M. Virulence Determinants and Multidrug Resistance of Escherichia coli Isolated from Migratory Birds. Antibiotics 2021, 10, 190. [Google Scholar] [CrossRef]
- Orubu, E.S.F.; Zaman, M.H.; Rahman, M.T.; Wirtz, V.J. Veterinary antimicrobial resistance containment in Bangladesh: Evaluating the national action plan and scoping the evidence on implementation. J. Glob. Antimicrob. Resist. 2020, 21, 105–115. [Google Scholar] [CrossRef] [PubMed]
- Etienne, M.; Lefebvre, E.; Frebourg, N.; Hamel, H.; Pestel-Caron, M.; Caron, F. Antibiotic treatment of acute uncomplicated cystitis based on rapid urine test and local epidemiology: Lessons from a primary care series. BMC Infect. Dis. 2014, 14, 1–8. [Google Scholar] [CrossRef] [Green Version]
- Nolan, L.K.; Vaillancourt, J.P.; Barbieri, N.L.; Logue, C.M. Colibacillosis. In Diseases of Poultry; John Wiley & Sons, Inc.: Hoboken, NJ, USA, 2020; pp. 770–830. [Google Scholar] [CrossRef]
- Subramanya, S.H.; Bairy, I.; Metok, Y.; Baral, B.P.; Gautam, D.; Nayak, N. Detection and characterization of ESBL-producing Enterobacteriaceae from the gut of subsistence farmers, their livestock, and the surrounding environment in rural Nepal. Sci. Rep. 2021, 11, 1–13. [Google Scholar]
- Ievy, S.; Islam, M.; Sobur, M.; Talukder, M.; Rahman, M.; Khan, M.F.R. Molecular detection of avian pathogenic Escherichia coli (APEC) for the first time in layer farms in Bangladesh and their antibiotic resistance patterns. Microorganisms 2020, 8, 1021. [Google Scholar] [CrossRef]
- Desvars-Larrive, A.; Ruppitsch, W.; Lepuschitz, S.; Szostak, M.P.; Spergser, J.; Feßler, A.T.; Schwarz, S.; Monecke, S.; Ehricht, R.; Walzer, C. Urban brown rats (Rattus norvegicus) as possible source of multidrug-resistant Enterobacteriaceae and meticillin-resistant Staphylococcus spp., Vienna, Austria, 2016 and 2017. Eurosurveillance 2019, 24, 1900149. [Google Scholar] [CrossRef] [Green Version]
- Gwenzi, W.; Chaukura, N.; Muisa-Zikali, N.; Teta, C.; Musvuugwa, T.; Rzymski, P.; Abia, A.L.K. Insects, Rodents, and Pets as Reservoirs, Vectors, and Sentinels of Antimicrobial Resistance. Antibiotics 2021, 10, 68. [Google Scholar] [CrossRef]
- Hassell, J.M.; Ward, M.J.; Muloi, D.; Bettridge, J.M.; Robinson, T.P.; Kariuki, S.; Ogendo, A.; Kiiru, J.; Imboma, T.; Kang’ethe, E.K.; et al. Clinically relevant antimicrobial resistance at the wildlife-livestock-human interface in Nairobi: An epidemiological study. Lancet Planet. Health 2019, 3, e259–e269. [Google Scholar] [CrossRef] [Green Version]
- Lupindu, A.M.; Dalsgaard, A.; Msoffe, P.L.; Ngowi, H.A.; Mtambo, M.M.; Olsen, J.E. Transmission of antibiotic-resistant Escherichia coli between cattle, humans and the environment in peri-urban livestock keeping communities in Morogoro, Tanzania. Prev. Vet. Med. 2015, 118, 477–482. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.-J.; Hu, H.-W.; Gou, M.; Wang, J.-T.; Chen, D.; He, J.-Z. Temporal succession of soil antibiotic resistance genes following application of swine, cattle and poultry manures spiked with or without antibiotics. Environ. Pollut. 2017, 231, 1621–1632. [Google Scholar] [CrossRef] [PubMed]
- Sanderson, H.; Brown, R.S.; Hania, P.; McAllister, T.A.; Majury, A.; Liss, S.N. Antimicrobial resistant genes and organisms as environmental contaminants of emerging concern: Addressing global public health risks. In Management of Emerging Public Health Issues and Risks; Elsevier: Amsterdam, The Netherlands, 2019; pp. 147–187. [Google Scholar]
- Touati, M.; Hadjadj, L.; Berrazeg, M.; Baron, S.A.; Rolain, J.M. Emergence of Escherichia coli harbouring mcr-1 and mcr-3 genes in North West Algerian farmlands. J. Glob. Antimicrob. Resist. 2020, 21, 132–137. [Google Scholar] [CrossRef] [PubMed]
- Guenther, S.; Bethe, A.; Fruth, A.; Semmler, T.; Ulrich, R.G.; Wieler, L.H.; Ewers, C. Frequent combination of antimicrobial multiresistance and extraintestinal pathogenicity in Escherichia coli isolates from urban rats (Rattus norvegicus) in Berlin, Germany. PLoS ONE 2012, 7, e50331. [Google Scholar] [CrossRef]
- Feng, A.Y.; Himsworth, C.G. The secret life of the city rat: A review of the ecology of urban Norway and black rats (Rattus norvegicus and Rattus rattus). Urban Ecosyst. 2014, 17, 149–162. [Google Scholar] [CrossRef]
- Kilonzo, B.; Mbise, T.; Mwalimu, D.; Kindamba, L. Observations on the endemicity of plague in Karatu and Ngorongoro, northern Tanzania. Tanzan. J. Health Res. 2006, 8, 1–6. [Google Scholar] [CrossRef] [Green Version]
- Makundi, R.H.; Massawe, A.W.; Borremans, B.; Laudisoit, A.; Katakweba, A. We are connected: Flea-host association networks in the plague outbreak focus in the Rift Valley, northern Tanzania. Wildl. Res. 2015, 42, 196–206. [Google Scholar] [CrossRef]
- Ziwa, M.H.; Matee, M.I.; Hang’ombe, B.M.; Lyamuya, E.F.; Kilonzo, B.S. Plague in Tanzania: An overview. Tanzan. J. Health Res. 2013, 15. [Google Scholar] [CrossRef] [Green Version]
- Haule, M.; Lyamuya, E.E.; Hang’ombe, B.M.; Matee, M.I. Investigation of Fleas as Vectors in the Transmission of Plague during a Quiescent Period in North-Eastern, Tanzania; Sokoine University of Agriculture: Morogoro, Tanzania, 2013. [Google Scholar]
- Makundi, R.H.; Massawe, A.W.; Mulungu, L.S.; Katakweba, A.; Mbise, T.J.; Mgode, G. Potential mammalian reservoirs in a bubonic plague outbreak focus in Mbulu District, northern Tanzania, in 2007. Mammalia 2008, 72, 253–257. [Google Scholar] [CrossRef]
- Rugumisa, B.; Call, D.R.; Mwanyika, G.O.; Subbiah, M.; Buza, J. Comparison of the Prevalence of Antibiotic-Resistant Escherichia coli Isolates from Commercial-Layer and Free-Range Chickens in Arusha District, Tanzania. 2016. Available online: https://dspace.nm-aist.ac.tz/handle/20.500.12479/457 (accessed on 20 June 2021).
- Lyimo, B.; Buza, J.; Subbiah, M.; Smith, W.; Call, D.R. Comparison of antibiotic resistant Escherichia coli obtained from drinking water sources in northern Tanzania: A cross-sectional study. BMC Microbiol. 2016, 16, 254. [Google Scholar] [CrossRef] [Green Version]
- Caudell, M.A.; Mair, C.; Subbiah, M.; Matthews, L.; Quinlan, R.J.; Quinlan, M.B.; Zadoks, R.; Keyyu, J.; Call, D.R. Identification of risk factors associated with carriage of resistant Escherichia coli in three culturally diverse ethnic groups in Tanzania: A biological and socioeconomic analysis. Lancet Planet. Health 2018, 2, e489–e497. [Google Scholar] [CrossRef] [Green Version]
- Kimera, Z.I.; Mgaya, F.X.; Misinzo, G.; Mshana, S.E.; Moremi, N.; Matee, M.I. Multidrug-Resistant, Including Extended-Spectrum Beta Lactamase-Producing and Quinolone-Resistant, Escherichia coli Isolated from Poultry and Domestic Pigs in Dar es Salaam, Tanzania. Antibiotics 2021, 10, 406. [Google Scholar] [CrossRef] [PubMed]
- Mgaya, F.X.; Matee, M.I.; Muhairwa, A.P.; Hoza, A.S. Occurrence of multidrug resistant Escherichia coli in raw meat and cloaca swabs in poultry processed in slaughter slabs in Dar es Salaam, Tanzania. Antibiotics 2021, 10, 343. [Google Scholar] [CrossRef]
- Gakuya, F.; Kyule, M.; Gathura, P.; Kariuki, S. Antimicrobial susceptibility and plasmids from Escherichia coli isolated from rats. East Afr. Med. J. 2001, 78, 518–522. [Google Scholar] [CrossRef] [Green Version]
- Himsworth, C.G.; Zabek, E.; Desruisseau, A.; Parmley, E.J.; Reid-Smith, R.; Jardine, C.M.; Tang, P.; Patrick, D.M. Prevalence and characteristics of Escherichia coli and Salmonella spp. in the feces of wild urban Norway and black rats (Rattus norvegicus and Rattus rattus) from an inner-city neighborhood of Vancouver, Canada. J. Wildl. Dis. 2015, 51, 589–600. [Google Scholar] [CrossRef]
- Le Huy, H.; Koizumi, N.; Ung, T.T.H.; Le, T.T.; Nguyen, H.L.K.; Hoang, P.V.M.; Nguyen, C.N.; Khong, T.M.; Hasebe, F.; Haga, T. Antibiotic-resistant Escherichia coli isolated from urban rodents in Hanoi, Vietnam. J. Vet. Med. Sci. 2020, 82, 653–660. [Google Scholar] [CrossRef] [Green Version]
- Montealegre, M.C.; Roy, S.; Böni, F.; Hossain, M.I.; Navab-Daneshmand, T.; Caduff, L.; Faruque, A.; Islam, M.A.; Julian, T.R. Risk factors for detection, survival, and growth of antibiotic-resistant and pathogenic Escherichia coli in household soils in rural Bangladesh. Appl. Environ. Microbiol. 2018, 84, e01978-18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Badowski, N.; Castro, C.M.; Montgomery, M.; Pickering, A.J.; Mamuya, S.; Davis, J. Understanding household behavioral risk factors for diarrheal disease in Dar es Salaam: A photovoice community assessment. J. Environ. Public Health 2011, 2011, 130467. [Google Scholar] [CrossRef]
- Pickering, A.J.; Julian, T.R.; Marks, S.J.; Mattioli, M.C.; Boehm, A.B.; Schwab, K.J.; Davis, J. Fecal contamination and diarrheal pathogens on surfaces and in soils among Tanzanian households with and without improved sanitation. Environ. Sci. Technol. 2012, 46, 5736–5743. [Google Scholar] [CrossRef] [PubMed]
- Sadiq, M.; Syed-Hussain, S.; Ramanoon, S.; Saharee, A.; Ahmad, N.; Zin, N.M.; Khalid, S.; Naseeha, D.; Syahirah, A.; Mansor, R. Knowledge, attitude and perception regarding antimicrobial resistance and usage among ruminant farmers in Selangor, Malaysia. Prev. Vet. Med. 2018, 156, 76–83. [Google Scholar] [CrossRef] [PubMed]
- Teklu, D.S.; Negeri, A.A.; Legese, M.H.; Bedada, T.L.; Woldemariam, H.K.; Tullu, K.D. Extended-spectrum beta-lactamase production and multi-drug resistance among Enterobacteriaceae isolated in Addis Ababa, Ethiopia. Antimicrob. Resist. Infect. Control 2019, 8, 39. [Google Scholar] [CrossRef]
- Mdegela, R.H.; Mwakapeje, E.R.; Rubegwa, B.; Gebeyehu, D.T.; Niyigena, S.; Msambichaka, V.; Nonga, H.E.; Antoine-Moussiaux, N.; Fasina, F.O. Antimicrobial Use, Residues, Resistance and Governance in the food and agriculture sectors, Tanzania. Antibiotics 2021, 10, 454. [Google Scholar] [CrossRef]
- Sindato, C.; Mboera, L.E.; Katale, B.Z.; Frumence, G.; Kimera, S.; Clark, T.G.; Legido-Quigley, H.; Mshana, S.E.; Rweyemamu, M.M.; Matee, M. Knowledge, attitudes and practices regarding antimicrobial use and resistance among communities of Ilala, Kilosa and Kibaha districts of Tanzania. Antimicrob. Resist. Infect. Control 2020, 9, 194. [Google Scholar] [CrossRef] [PubMed]
- Arnold, K.E.; Williams, N.J.; Bennett, M. ‘Disperse abroad in the land’: The role of wildlife in the dissemination of antimicrobial resistance. Biol. Lett. 2016, 12, 20160137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- URT (United Republic of Tanzania). 2012 Population and Housing Census—Population Distribution by Administrative Areas; URT: Dodoma, Tanzania, 2013; p. 244. [Google Scholar]
- Quinn, P.J.; Markey, B.K.; Carter, M.E.; Donnelly, W.J.; Leonard, F.C. Veterinary Microbiology and Microbial Disease: Pathogenic Bacteria Blackwell Scientific Publications; Oxford: London, UK, 2002; pp. 113–115. [Google Scholar]
- CLSI. Clinical and Laboratory Standards Institute-Performance Standards for Antimicrobial Susceptibility Testing; CLSI: Wayne, PA, USA, 2020. [Google Scholar]
- Magiorakos, A.-P.; Srinivasan, A.; Carey, R.; Carmeli, Y.; Falagas, M.; Giske, C.; Harbarth, S.; Hindler, J.; Kahlmeter, G.; Olsson-Liljequist, B. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 2012, 18, 268–281. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Type of Samples | Total Number of Samples n (%) | Positive Samples n (%) | Chi-Square | p-Value |
---|---|---|---|---|
Chickens | 288 (30.0) | 236 (81.9) | X2 = 147.58, df = 3 | <0.001 |
Humans | 281 (29.3) | 243 (86.5) | ||
Rodents | 101 (10.5) | 81 (80.2) | ||
Soil | 290 (30.2) | 90 (31.0) | ||
Total | 960 (100.0) | 650 (67.7) |
Types of Sample Sources | Number of Antibiotic Classes to Which the Isolates Were Resistant, n (%) | Total Number of Isolates | MDR Isolates (3–6 Classes) | Chi-Square | p-Value | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|
0 | 1 | 2 | 3 | 4 | 5 | 6 | |||||
Overall n (%) | 5 (0.8) | 24 (3.7) | 109 (16.8) | 249 (38.3) | 163 (25.1) | 84 (12.9) | 16 (2.5) | 650 (100.0) | 512 (78.8) | ||
Chickens | 0 (0.0) | 10 (1.5) | 46 (7.1) | 103 (15.8) | 55 (8.5) | 15 (2.3) | 7 (1.1) | 236 (36.3) | 180 (27.7) | 129.75 df = 3 | <0.001 |
Humans | 5 (0.8) | 8 (1.2) | 33 (5.1) | 88 (13.5) | 63 (9.7) | 41 (6.3) | 5 (0.8) | 243 (37.4) | 197 (30.3) | 75.47, df = 3 | <0.001 |
Rodents | 0 (0.0) | 2 (0.3) | 9 (1.4) | 25 (3.8) | 20 (3.1) | 22 (3.4) | 3 (0.5) | 81 (12.5) | 70 (10.8) | 16.16, df = 3 | 0.001 |
Soil | 0 (0.0) | 4 (0.6) | 21 (3.2) | 33 (5.1) | 25 (3.8) | 6 (0.9) | 1 (0.2) | 90 (13.8) | 65 (10.0) | 42.75, df = 3 | <0.001 |
Ward | Types of Sample Sources, n (%) | MDR Isolates | Chi-Square | p-Value | |||
---|---|---|---|---|---|---|---|
Chickens | Humans | Rodents | Soil | ||||
Overall n (%) | 180 (27.7) | 197 (30.3) | 70 (10.8) | 65 (10.0) | 512 (78.8) | ||
Endabash | 20 (3.1) | 22 (3.4) | 17 (2.6) | 15 (2.3) | 74 (11.4) | 1.6571, df = 3 | 0.647 |
Endamarariek | 32 (4.9) | 27 (4.2) | 10 (1.5) | 12 (1.8) | 81 (12.5) | 18.532, df = 3 | <0.001 |
Karatu | 40 (6.2) | 61 (9.4) | 24 (3.7) | 12 (1.8) | 137 (21.1) | 49.118, df = 3 | <0.001 |
Mbulumbulu | 50 (7.7) | 42 (6.5) | 8 (1.8) | 16 (2.5) | 116 (17.8) | 43.571, df = 3 | <0.001 |
Rhotia | 38 (5.8) | 45 (6.9) | 11 (1.7) | 10 (1.5) | 104 (16.0) | 39.44, df = 3 | <0.001 |
Chi-Square | 24.82, df = 4 | 25.03, df = 4 | 13.077, df = 4 | 2.00, df = 4 | |||
p-value | <0.001 | <0.001 | 0.011 | 0.736 |
Chicken Samples | Number of Isolates (n) | Occurrence (%) | Antibiotic Resistance Patterns | Number of Antibiotic Classes |
---|---|---|---|---|
(n = 180) | 10 | 1.5 | AMC, IMP, CTX | 3 |
9 | 1.4 | IMP, CIP, CTX | ||
1 | 0.2 | AMC, IMP, CIP | ||
2 | 0.3 | AMC, CIP, CTX | ||
3 | 0.5 | TE, AMC, CTX | ||
2 | 0.3 | TE, AMC, IMP | ||
4 | 0.6 | TE, CIP, CTX | ||
48 | 7.4 | TE, IMP, CTX | ||
1 | 0.2 | TE, IMP, CIP | ||
2 | 0.3 | TE, AMC, CTX | ||
12 | 1.8 | TE, CIP, CTX | ||
2 | 0.3 | TE, IMP, CIP | ||
3 | 0.5 | TE, CIP, CTX | ||
2 | 0.3 | TE, AMC, IMP | ||
1 | 0.2 | TE, IMP, CN | ||
1 | 0.2 | TE, AMC, CIP | ||
1 | 0.2 | TE, CIP, CTX, CN | 4 | |
2 | 0.3 | AMC, IMP, CTX, CN | ||
4 | 0.6 | AMC, IMP, CIP, CTX, | ||
23 | 3.5 | TE, IMP, CIP, CTX | ||
1 | 0.2 | TE, IMP, CIP, CN | ||
20 | 3.1 | TE, AMC, CIP, CTX | ||
2 | 0.3 | TE, AMC, IMP, CTX | ||
2 | 0.3 | TE, IMP, CTX, CN | ||
10 | 1.5 | TE, AMC, IMP, CIP, CTX | 5 | |
3 | 0.5 | TE, IMP, CIP, CTX, CN | ||
1 | 0.2 | TE, AMC, IMP, CTX, CN | ||
1 | 0.2 | TE, IMP, CIP, CTX, CN | ||
7 | 1.1 | TE, AMC, IMP, CIP, CTX, CN | 6 | |
Total | 180 | 27.7 |
Human Samples | Number of Isolates (n) | Occurrence (%) | Antibiotic Resistance Patterns | Number of Antibiotic Classes |
---|---|---|---|---|
(n = 197) | 17 | 2.6 | AMC, IMP, CTX | 3 |
5 | 0.8 | AMC, IMP, CIP | ||
2 | 0.3 | AMC, CIP, CTX | ||
29 | 4.5 | TE, IMP, CTX | ||
10 | 1.5 | TE, AMC, CTX | ||
1 | 0.2 | IMP, CIP, CTX | ||
8 | 1.2 | TE, AMC, IMP | ||
7 | 1.1 | TE, IMP, CIP | ||
2 | 0.3 | TE, AMC, CIP | ||
2 | 0.3 | TE, CIP, CTX | ||
2 | 0.3 | TE, CTX, CN | ||
1 | 0.2 | TE, IMP, CTX | ||
1 | 0.2 | TE, CIP, CTX | ||
1 | 0.2 | TE, IMP, CN | ||
6 | 0.9 | TE, AMC, IMP, CIP | 4 | |
1 | 0.2 | IMP, CIP, CTX, CN | ||
1 | 0.2 | TE, AMC, IMP, CN | ||
1 | 0.2 | TE, AMC, CTX, CN | ||
1 | 0.2 | AMC, IMP, CTX, CN | ||
1 | 0.2 | AMC, IMP, CIP, CN | ||
32 | 4.9 | TE, AMC, IMP, CTX | ||
4 | 0.6 | TE, AMC, CIP, CTX | ||
9 | 1.4 | TE, IMP, CIP, CTX | ||
7 | 1.1 | AMC, IMP, CIP, CTX | ||
33 | 5.1 | TE, AMC, IMP, CIP, CTX | 5 | |
1 | 0.2 | AMC, IMP, CIP, CTX, CN | ||
4 | 0.6 | TE, AMC, IMP, CTX, CN | ||
2 | 0.3 | TE, IMP, CIP, CTX, CN | ||
1 | 0.2 | TE, AMC, CIP, CTX, CN | ||
5 | 0.8 | TE, AMC, IMP, CIP, CTX, CN | 6 | |
Total | 197 | 30.3 |
Rodent Samples | Number of Isolates (n) | Occurrence (%) | Antibiotic Resistance Patterns | Number of Antibiotic Classes |
---|---|---|---|---|
(n = 70) | 3 | 0.5 | AMC, IMP, CIP | 3 |
4 | 0.6 | AMC, CIP, CTX | ||
1 | 0.2 | AMC, IMP, CTX | ||
1 | 0.2 | IMP, CIP, CTX | ||
8 | 1.2 | TE, IMP, CTX | ||
1 | 0.2 | TE, AMC, IMP | ||
1 | 0.2 | TE, CIP, CTX | ||
1 | 0.2 | TE, AMC, CTX | ||
1 | 0.2 | TE, AMC, IMP | ||
3 | 0.5 | TE, IMP, CIP | ||
2 | 0.3 | AMC, IMP, CIP, CTX | 4 | |
9 | 1.4 | TE, AMC, IMP, CTX | ||
1 | 0.2 | TE, AMC, CIP, CN | ||
3 | 0.5 | TE, IMP, CIP, CTX | ||
5 | 0.8 | TE, AMC, IMP CIP | ||
22 | 3.4 | TE, AMC, IMP, CIP, CTX | 5 | |
1 | 0.2 | TE, AMC, IMP, CIP, CN | ||
3 | 0.5 | TE, AMC, IMP, CIP, CTX, CN | 6 | |
Total | 70 | 10.8 |
Source of Samples | Number of Isolates (n) | Occurrence (%) | Antibiotic Resistance Patterns | Number of Antibiotic Classes |
---|---|---|---|---|
(n = 512) | 1 | 0.2 | AMC, IMP, CIP | 3 |
7 | 1.1 | AMC, IMP, CTX | ||
3 | 0.5 | AMC, IMP, CTX | ||
1 | 0.2 | IMP, CIP, CTX, CN | ||
1 | 0.2 | IMP, CTX, CN | ||
3 | 0.5 | TE, AMC, CTX | ||
1 | 0.2 | TE, AMC, CIP | ||
1 | 0.2 | TE, CIP, CTX | ||
2 | 0.3 | TE, IMP, CIP | ||
13 | 2.0 | TE, IMP, CTX | ||
12 | 1.8 | TE, AMC, IMP, CTX | 4 | |
4 | 0.6 | TE, IMP, CIP, CTX | ||
4 | 0.6 | TE, AMC, CIP, CTX | ||
4 | 0.6 | AMC, IMP, CIP, CTX | ||
1 | 0.2 | TE, IMP, CTX, CN | ||
1 | 0.2 | AMC, IMP, CIP, CTX, CN | 5 | |
1 | 0.2 | TE, IMP, CIP, CTX, CN | ||
4 | 0.6 | TE, AMC, IMP, CIP, CN | ||
1 | 0.2 | TE, AMC, IMP, CIP, CTX, CN | 6 | |
Total | 65 | 10.0 |
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Sonola, V.S.; Katakweba, A.S.; Misinzo, G.; Matee, M.I.N. Occurrence of Multi-Drug-Resistant Escherichia coli in Chickens, Humans, Rodents and Household Soil in Karatu, Northern Tanzania. Antibiotics 2021, 10, 1137. https://doi.org/10.3390/antibiotics10091137
Sonola VS, Katakweba AS, Misinzo G, Matee MIN. Occurrence of Multi-Drug-Resistant Escherichia coli in Chickens, Humans, Rodents and Household Soil in Karatu, Northern Tanzania. Antibiotics. 2021; 10(9):1137. https://doi.org/10.3390/antibiotics10091137
Chicago/Turabian StyleSonola, Valery S., Abdul S. Katakweba, Gerald Misinzo, and Mecky I. N. Matee. 2021. "Occurrence of Multi-Drug-Resistant Escherichia coli in Chickens, Humans, Rodents and Household Soil in Karatu, Northern Tanzania" Antibiotics 10, no. 9: 1137. https://doi.org/10.3390/antibiotics10091137
APA StyleSonola, V. S., Katakweba, A. S., Misinzo, G., & Matee, M. I. N. (2021). Occurrence of Multi-Drug-Resistant Escherichia coli in Chickens, Humans, Rodents and Household Soil in Karatu, Northern Tanzania. Antibiotics, 10(9), 1137. https://doi.org/10.3390/antibiotics10091137