Prevalence of Multidrug-Resistant Pseudomonas aeruginosa Isolated from Dairy Cattle, Milk, Environment, and Workers’ Hands
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design
2.2. Origins and Processing of Samples
2.2.1. Animal Samples
2.2.2. Environmental Samples
2.2.3. Human Samples
2.3. Animal-House Description
2.4. Bacteriological and Chemical Identification of P. aeruginosa Strains
2.5. Molecular Identification of P. aeruginosa via 16S rRNA Gene Detection
2.6. Phenotypic AMR of Farms and Households’ Strains of P. aeruginosa
2.7. Molecular Identification of P. aeruginosa AMR-Resistance Genes (ARGs)
2.8. Statistical Analysis
3. Results
3.1. Prevalence of P. aeruginosa Isolated from Three Examined Dairy Farms and Households
3.2. AMR of P. aeruginosa Recovered from Different Sources
4. Discussion
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Target Gene | Primer Sequence (5′–3′) | Amplified Segment (bp) | Primary Denaturation | Amplification (35 Cycles) | Final Extension | Reference | ||
---|---|---|---|---|---|---|---|---|
16S rRNA | GGGGGATCTTCGGACCTCA TCCTTAGAGTGCCCACCCG | 956 | 94 °C/5 min | 94 °C/30 s | 58 °C/40 s | 72 °C/45 s | 72 °C/10 min | [12] |
sul1 | CGGCGTGGGCTACCTGAACG GCCGATCGCGTGAAGTTCCG | 433 | 94 °C/5 min | 94 °C/30 s | 60 °C/40 s | 72 °C/45 s | 72 °C/10 min | [13] |
drfA | TGGTAGCTATATCGAAGAATGGAGT TATGTTAGAGGCGAAGTCTTGGGTA | 425 | 94 °C/5 min | 94 °C30 s | 60 °C/40 s | 72 °C/45 s | 72 °C/10 min | [14] |
ermB | CATTTAACGACGAAACTGGC GGAACATCTGTGGTATGGCG | 425 | 94 °C/5 min | 94 °C/30 s | 51 °C/40 s | 72 °C/45 s | 72 °C/10 min | [15] |
Samples | Farm I | Farm II | Farm III | Total of Examined Farms (n = 3) | ||||
---|---|---|---|---|---|---|---|---|
Total No. | Positive No. (%) | Total No. | Positive No. (%) | Total No. | Positive No. (%) | Total No. | Positive No. (%) | |
Animal | 60 | 13 (21.7) | 33 | 6 (18.2) | 55 | 4 (7.3) | 148 | 23 (15.6) |
Rectal swabs | 20 | 5 (25) | 13 | 3 (23.1) | 20 | 3 (15) | 53 | 11 (20.8) |
Milk | 20 | 3 (15) | 10 | 1 (10) | 20 | 1 (5) | 50 | 5 (10) |
Udder skin swabs | 20 | 5 (25) | 10 | 2 (20) | 15 | 0 (0) | 45 | 7 (15.6) |
Environment | 60 | 4 (6.7) | 22 | 3 (13.6) | 45 | 2 (4.4) | 127 | 9 (7.1) |
Drinking water | 15 | 2 (13.3) | 6 | 1 (16.7) | 10 | 1 (10) | 31 | 3 (9.7) |
Water source | 15 | 1 (6.7) | 6 | 1 (16.7) | 15 | 0 (0) | 36 | 3 (8.3) |
Feedstuff | 15 | 0 (0) | 5 | 0 (0) | 10 | 0 (0) | 30 | 0 (0) |
Bedding | 15 | 1 (6.7) | 5 | 1 (20) | 10 | 1 (10) | 30 | 3 (10) |
Human (hand swabs) | 15 | 1 (6.7) | 10 | 0 (0) | 20 | 0 (0) | 45 | 1 (2.2) |
Total | 135 | 18 (13.3) | 65 | 9 (16.4) | 120 | 6 (5) | 320 | 33 (10.3) |
p value | p = 0.267 | p = 0.914 | p = 0.36 | p = 0.045 * |
Samples | Household I | Household II | Household III | Total of Examined Household (n = 3) | ||||
---|---|---|---|---|---|---|---|---|
Total n | Positive n (%) | Total n | Positive n (%) | Total n | Positive n (%) | Total n | Positive n (%) | |
Animal | 15 | 11 (73.3) | 15 | 8 (53.3) | 15 | 9 (60) | 45 | 28 (62.2) |
Rectal swabs | 5 | 3 (60) | 5 | 5 (100) | 5 | 2 (40) | 15 | 10 (66.7) |
Milk | 5 | 4 (80) | 5 | 1 (20) | 5 | 3 (60) | 15 | 8 (53.3) |
Udder skin swabs | 5 | 4 (80) | 5 | 2 (40) | 5 | 4 (80) | 15 | 10 (66.7) |
Environment | 20 | 14 (70) | 20 | 14 (70) | 20 | 9 (45) | 60 | 37 (61.7) |
Drinking water | 5 | 4 (80) | 5 | 5 (100) | 5 | 2 (40) | 15 | 11 (73.3) |
Water source | 5 | 3 (60) | 5 | 3 (60) | 5 | 1 (20) | 15 | 7 (46.7) |
Feedstuff | 5 | 5 (100) | 5 | 3 (60) | 5 | 3 (60) | 15 | 11 (73.3) |
Bedding | 5 | 2 (40) | 5 | 3 (60) | 5 | 3 (60) | 15 | 8 (53.3) |
Human (hand swabs) | 5 | 1 (20) | 5 | 2 (40) | 5 | 1 (20) | 15 | 4 (26.7) |
Total | 35 | 25 (71.7) | 40 | 24 (60) | 40 | 19 (47.5) | 120 | 69 (57.5) |
p value | p = 0.813 | p = 0.402 | p = 0.287 | p = 0.546 * |
Samples | Total No. of Isolates | Distribution of Antimicrobial Resistance Amongst Strains | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
E | G | AK | CP | NOR | SXT | IMP | AX | CPM | LEV | TZP | |||
Farm I | Animal | 13 | 6 | 11 | 6 | 2 | 0 | 13 | 9 | 4 | 10 | 3 | 7 |
Environment | 4 | 1 | 3 | 0 | 0 | 0 | 4 | 3 | 2 | 3 | 0 | 4 | |
Human | 1 | 1 | 1 | 1 | 0 | 0 | 1 | 1 | 1 | 1 | 1 | 1 | |
Total | 18 | 8 | 15 | 7 | 2 | 0 | 18 | 13 | 7 | 14 | 4 | 12 | |
Farm II | Animal | 6 | 5 | 4 | 4 | 1 | 0 | 6 | 5 | 5 | 4 | 1 | 5 |
Environment | 3 | 0 | 0 | 0 | 1 | 0 | 3 | 3 | 3 | 2 | 0 | 2 | |
Human | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
Total | 9 | 5 | 4 | 4 | 2 | 0 | 9 | 8 | 8 | 6 | 1 | 7 | |
Farm III | Animal | 4 | 1 | 2 | 0 | 1 | 3 | 4 | 1 | 1 | 3 | 2 | 2 |
Environment | 2 | 0 | 0 | 0 | 0 | 0 | 2 | 2 | 2 | 1 | 2 | 1 | |
Human | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
Total | 6 | 1 | 2 | 0 | 1 | 3 | 6 | 3 | 3 | 4 | 4 | 3 | |
Total | 33 | 13 | 21 | 11 | 5 | 3 | 33 | 24 | 18 | 24 | 9 | 22 | |
Resistance % | 100% | 39.4 | 63.3 | 33.3 | 15 | 9.1 | 100 | 72.7 | 54.5 | 72.7 | 27.3 | 68.8 |
Samples | Total No. of Positive | Distribution of Antimicrobial Resistance Amongst Strains | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
E | G | AK | CP | NOR | SXT | IMP | AX | CPM | LEV | TZP | |||
Household I | Animal | 11 | 2 | 9 | 4 | 0 | 2 | 11 | 9 | 9 | 7 | 2 | 8 |
Environment | 14 | 3 | 5 | 4 | 0 | 1 | 14 | 12 | 12 | 10 | 4 | 7 | |
Human | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | |
Total | 26 | 5 | 14 | 8 | 0 | 3 | 26 | 21 | 21 | 18 | 6 | 15 | |
household II | Animal | 8 | 7 | 6 | 1 | 0 | 4 | 8 | 7 | 7 | 4 | 5 | 3 |
Environment | 14 | 14 | 14 | 0 | 0 | 9 | 14 | 10 | 10 | 9 | 11 | 7 | |
Human | 2 | 2 | 2 | 0 | 0 | 0 | 2 | 2 | 2 | 2 | 0 | 0 | |
Total | 24 | 23 | 22 | 1 | 0 | 13 | 24 | 19 | 19 | 15 | 16 | 10 | |
Household III | Animal | 9 | 9 | 9 | 0 | 0 | 3 | 6 | 8 | 8 | 9 | 5 | 2 |
Environment | 9 | 7 | 7 | 2 | 0 | 0 | 6 | 8 | 4 | 5 | 3 | 0 | |
Human | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | |
Total | 19 | 16 | 16 | 2 | 0 | 3 | 13 | 17 | 12 | 14 | 8 | 2 | |
Total | 69 | 44 | 52 | 11 | 0 | 19 | 63 | 57 | 52 | 47 | 30 | 27 | |
Resistance % | 100 | 63.8 | 75.4 | 15.9 | 0 | 27.5 | 91.3 | 82.6 | 75.4 | 68.1 | 43.5 | 39.1 |
Source | Sample | Antimicrobial Profile | MAR Index | Distribution of Antibiotic Resistance Genes | ||||
---|---|---|---|---|---|---|---|---|
Farm No. | Type | ID | Type | drfA | sul1 | ermB | ||
Farm I | Animal | 2 | Rectal swab | SXT, E, G, AK, IMP, CPM, TZP | 0.636 MDR | + | + | + |
6 | Rectal swab | SXT, E, G, IMP, AX, CPM | 0.545 MDR | + | + | + | ||
7 | Rectal swab | SXT, E, G, AK, CP, CPM | 0.545 MDR | + | + | + | ||
13 | Rectal swab | SXT, G, IMP, AX, CPM | 0.454 MDR | + | ||||
19 | Rectal swab | SXT, G, AK, IMP, AX, CPM, LEV | 0.636 MDR | + | ||||
33 | Milk | SXT, G, AK, CPM, LEV | 0.454 MDR | + | ||||
35 | Milk | SXT, E, G, AK, IMP, AX, CPM, TZP | 0.727 MDR | + | ||||
39 | Milk | SXT, G, IMP, TZP | 0.363 MDR | + | ||||
44 | Rectal swab | SXT, G, AK, CPM, TZP | 0.454 MDR | + | ||||
50 | Rectal swab | SXT, G, IMP | 0.272 | + | ||||
51 | Rectal swab | SXT, IMP, CPM, TZP | 0.363 MDR | + | ||||
53 | Rectal swab | SXT, E, IMP, TZP | 0.363 | + | + | |||
56 | Rectal swab | SXT, E, G, CP, CPM, LEV, TZP | 0.636 MDR | + | + | |||
Environment | 66 | Drinking water | SXT, G, IMP, CPM, TZP | 0.454 MDR | + | + | ||
67 | Drinking water | SXT, G, TZP | 0.272 | + | + | |||
73 | Drinking water | SXT, E, G, IMP, AX, CPM, TZP | 0.636 MDR | + | + | |||
89 | Bedding | SXT, G, IMP, AX, CPM, TZP | 0.545 MDR | + | ||||
101 | Hand swab | SXT, E, G, AK, IMP, AX, CPM, LEV, TZP | 0.818 MDR | + | + | + | ||
Farm II | Animal | 115 | Rectal swab | SXT, G, AK, IMP, AX, CPM, TZP | 0.636 MDR | + | ||
119 | Rectal swab | SXT, G, AK, IMP, AX, TZP | 0.545 MDR | + | ||||
120 | Rectal swab | SXT, E, AK, IMP, AX, CPM, TZP | 0.636 MDR | + | + | + | ||
139 | Milk | SXT, E, G, AK, IMP, CPM, LEV, TZP | 0.727 MDR | + | + | + | ||
161 | Udder skin swab | SXT, E, IMP, AX, TZP | 0.454 | + | + | |||
163 | Udder skin swab | SXT, E, G, CP, AX, CPM | 0.545 MDR | + | + | + | ||
Environment | 177 | Drinking water | SXT, CP, IMP, AX, CPM, TZP | 0.545 MDR | + | |||
183 | Water source | SXT, IMP, AX | 0.272 | + | ||||
185 | Bedding | SXT, IMP, AX, CPM, TZP | 0.454 MDR | + | ||||
Farm III | Animal | 201 | Rectal swab | SXT, IMP, AX, LEV, TZP | 0.454 MDR | + | ||
213 | Rectal swab | SXT, E, G, CP, NOR, CPM | 0.545 MDR | + | + | |||
224 | Rectal swab | SXT, CP, NOR, CPM | 0.363 | + | ||||
246 | Milk | SXT, G, NOR, CPM, LEV, TZP | 0.545 MDR | + | ||||
Environment | 287 | Drinking water | SXT, IMP, AX, LEV | 0.363 | + | |||
292 | Bedding | SXT, IMP, AX, CPM, LEV, TZP | 0.545 MDR | + |
Source | Sample | Antimicrobial Resistance Profile | MAR Index | Distribution of Antibiotic Resistance Genes | ||||
---|---|---|---|---|---|---|---|---|
Household No. | Type | ID | Type | drfA | sul1 | ermB | ||
Household I | Animal | 311 | Rectal swab | G, SXT, IMP, AX, CPM | 0.454 MDR | + | ||
312 | Rectal swab | G, SXT, IMP, AX, TZP | 0.454 MDR | + | ||||
314 | Rectal swab | AK, SXT, IMP, AX, CPM, LEV | 0.545 MDR | + | ||||
316 | Milk | G, SXT, IMP, AX, TZP | 0.454 MDR | + | ||||
317 | Milk | SXT, IMP, AX, CPM, TZP | 0.454 MDR | + | ||||
318 | Milk | G, SXT, IMP, AX, CPM, TZP | 0.545 MDR | + | ||||
319 | Milk | G, AK, SXT, IMP, AX, CPM, LEV | 0.636 MDR | + | ||||
322 | Udder skin swab | E, G, AK, NOR, SXT, CPM, TZP | 0.636 MDR | + | + | + | ||
323 | Udder skin swab | G, SXT, IMP, AX, TZP | 0.454 MDR | + | ||||
324 | Udder skin swab | G, SXT, IMP, AX, TZP | 0.454 MDR | + | ||||
325 | Udder skin swab | E, G, AK, NOR, SXT, CPM, TZP | 0.636 MDR | + | + | + | ||
Environment | 326 | Drinking water | G, AK, SXT, CPM, LEV, TZP | 0.545 MDR | + | + | ||
328 | Drinking water | G, SXT, IMP, AX, CPM, LEV, TZP | 0.636 MDR | + | ||||
329 | Drinking water | AK, SXT, IMP, AX, CPM, TZP | 0.545 MDR | + | + | |||
330 | Drinking water | SXT, IMP, AX, CPM, LEV | 0.454 MDR | + | ||||
331 | Water source | E, G, SXT, IMP, AX, CPM, LEV, TZP | 0.727 MDR | + | + | |||
333 | Water source | E, G, AK, SXT, IMP, AX, CPM | 0.636 MDR | + | + | |||
334 | Water source | NOR, SXT, IMP, AX, CPM | 0.454 MDR | + | + | |||
336 | Feedstuff | SXT, IMP, AX, CPM, TZP | 0.454 MDR | + | ||||
337 | Feedstuff | SXT, IMP, AX, CPM, TZP | 0.454 MDR | + | ||||
338 | Feedstuff | SXT, IMP, AX, TZP | 0.363 | + | ||||
339 | Feedstuff | SXT, IMP, AX | 0.272 | + | ||||
340 | Feedstuff | SXT, IMP, AX | 0.272 | + | ||||
343 | Bedding | SXT, IMP, AX | 0.272 | + | ||||
345 | Bedding | E, G, AK, SXT, CPM | 0.454 | + | + | + | ||
Human | 349 | Hand swab | SXT, CPM | 0.181 | + | + | ||
Household II | Animal | 351 | Rectal swab | SXT, IMP, AX, LEV, TZP | 0.454 MDR | + | + | |
352 | Rectal swab | E, AK, SXT, IMP, AX, LEV, TZP | 0.636 MDR | + | + | |||
353 | Rectal swab | E, G, SXT, IMP, AX, CPM | 0.545 MDR | + | + | |||
354 | Rectal swab | E, G, NOR, SXT, IMP, AX, CPM, LEV | 0.727 MDR | + | ||||
355 | Rectal swab | E, G, NOR, SXT, IMP, AX | 0.545 | + | ||||
360 | Milk | E, G, NOR, SXT, IMP, AX, LEV, TZP | 0.727 MDR | + | + | + | ||
362 | Udder skin swab | E, G, SXT, CPM, LEV | 0.454 MDR | |||||
364 | Udder skin swab | E, G, NOR, SXT, IMP, AX, CPM | 0.636 MDR | + | + | |||
Environment | 366 | Drinking water | E, G, NOR, SXT, IMP, AX, CPM, LEV | 0.727 MDR | + | + | + | |
367 | Drinking water | E, G, SXT, IMP, AX, CPM, LEV, TZP | 0.727 MDR | + | + | + | ||
368 | Drinking water | E, G, SXT, IMP, AX, LEV, TZP | 0.636 MDR | + | ||||
369 | Drinking water | E, G, NOR, SXT, IMP, AX, CPM, LEV | 0.727 MDR | + | ||||
370 | Drinking water | E, G, SXT, CPM, LEV, TZP | 0.545 MDR | + | + | + | ||
371 | Water source | E, G, NOR, SXT, IMP, AX, CPM, LEV | 0.727 MDR | + | + | |||
372 | Water source | E, G, NOR, SXT, CPM, LEV, TZP | 0.636 MDR | |||||
374 | Water source | E, G, NOR, SXT | 0.363 | + | + | + | ||
378 | Feedstuff | E, G, SXT, CPM, LEV | 0.454 MDR | + | + | |||
379 | Feedstuff | E, G, NOR, SXT, IMP, AX | 0.545 | + | + | |||
380 | Feedstuff | E, G, SXT, IMP, AX, CPM, LEV, TZP | 0.727 MDR | + | ||||
381 | Bedding | E, G, NOR, SXT, IMP, AX, CPM, TZP | 0.727 MDR | + | ||||
384 | Bedding | E, G, NOR, SXT, IMP, AX, LEV, TZP | 0.727 MDR | + | + | |||
385 | Bedding | E, G, NOR, SXT, IMP, AX, LEV | 0.636 MDR | + | + | |||
Human | 386 | Hand swab | E, G, SXT, IMP, AX, CPM | 0.545 MDR | + | + | + | |
388 | Hand swab | E, G, SXT, IMP, AX, CPM | 0.545 MDR | + | + | + | ||
household III | Animal | 393 | Rectal swab | E, G, IMP, AX, SXT, CPM | 0.545 MDR | + | + | + |
395 | Rectal swab | E, G, IMP, AX, SXT, CPM | 0.545 MDR | + | + | |||
398 | Milk | E, G, IMP, AX, SXT, CPM, LEV, TZP | 0.727 MDR | + | + | |||
399 | Milk | E, G, IMP, AX, SXT, CPM, LEV | 0.636 MDR | + | + | + | ||
400 | Milk | E, G, IMP, AX, SXT, CPM | 0.545 MDR | + | + | |||
402 | Udder skin swab | E, G, NOR, IMP, AX, SXT, CPM, LEV, TZP | 0.818 MDR | + | + | |||
403 | Udder skin swab | E, G, NOR, IMP, AX, CPM, LEV | 0.636 MDR | + | ||||
404 | Udder skin swab | E, G, NOR, IMP, AX, CPM | 0.545 MDR | + | ||||
405 | Udder skin swab | E, G, CPM, LEV | 0.363 MDR | + | ||||
Environment | 406 | Drinking water | E, G, IMP, AX, CPM | 0.454 MDR | + | |||
410 | Drinking water | E, G, IMP, AX, CPM, LEV | 0.545 MDR | + | ||||
415 | Water source | E, G, IMP, AX, CPM | 0.454 MDR | + | ||||
418 | Feedstuff | E, AK, SXT, IMP, LEV | 0.454 MDR | + | + | + | ||
419 | Feedstuff | E, G, SXT, IMP, CPM | 0.454 MDR | + | + | |||
420 | Feedstuff | G, SXT, IMP | 0272 | + | ||||
421 | Bedding | SXT | 0.090 | + | + | |||
423 | Bedding | E, G, IMP, AX, LEV | 0.454 MDR | + | ||||
425 | Bedding | E, G, AK, SXT, CPM | 0.454 MDR | + | + | + | ||
Human | 427 | Hand swab | SXT, IMP | 0.181 | + | + |
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Badawy, B.; Moustafa, S.; Shata, R.; Sayed-Ahmed, M.Z.; Alqahtani, S.S.; Ali, M.S.; Alam, N.; Ahmad, S.; Kasem, N.; Elbaz, E.; et al. Prevalence of Multidrug-Resistant Pseudomonas aeruginosa Isolated from Dairy Cattle, Milk, Environment, and Workers’ Hands. Microorganisms 2023, 11, 2775. https://doi.org/10.3390/microorganisms11112775
Badawy B, Moustafa S, Shata R, Sayed-Ahmed MZ, Alqahtani SS, Ali MS, Alam N, Ahmad S, Kasem N, Elbaz E, et al. Prevalence of Multidrug-Resistant Pseudomonas aeruginosa Isolated from Dairy Cattle, Milk, Environment, and Workers’ Hands. Microorganisms. 2023; 11(11):2775. https://doi.org/10.3390/microorganisms11112775
Chicago/Turabian StyleBadawy, Basma, Samar Moustafa, Radwa Shata, Mohamed Z. Sayed-Ahmed, Saad S. Alqahtani, Md Sajid Ali, Nawazish Alam, Sarfaraz Ahmad, Nahed Kasem, Elzahara Elbaz, and et al. 2023. "Prevalence of Multidrug-Resistant Pseudomonas aeruginosa Isolated from Dairy Cattle, Milk, Environment, and Workers’ Hands" Microorganisms 11, no. 11: 2775. https://doi.org/10.3390/microorganisms11112775