Abstract
Integrated broiler operations that allow producers to combine various biosecurity and sanitation practices account for approximately 97.6% of chicken meat production in Korea, but it is not well known about the biosecurity level or compliance with regulations for each operation. Therefore, the objective this study was to analyze the current adoption of biosecurity practices and trends in antimicrobial use in 74 farms from 5 major integrated broiler chicken operations (A–E). The highest stock densities of more than 65 birds per 3.3 m2 (0.5 birds/ft2) showed in 66.7 and 33.3% of the farms in operations A and C, respectively. Also, the livability rate of 98% or less was observed in 73.3 and 93.4% of the farms, in operation A and C, respectively, which lower than other operations. Moreover, it was observed that 60.0 and 40.0% of farms in operations B and C reused litter 3 or more times. Among the 74 farms, the most common antimicrobials prescription frequency was 2 times (39.2%), and the prescription to β-lactams antibiotics (45.3%) showed the significantly highest (P < 0.05). The highest administration of antimicrobials was at 15 to 22-days old (42.7%), and most of them were recommended by veterinarian (80.7%). Footbath disinfectant and spraying outside the poultry house were performed in most of the farms (64.9 and 83.8%, respectively), but the use of quicklime (36.5%) and drinking water disinfectant (18.9%) was low in farms. Most of the farms washed vehicles for transportation of poultry (87.8%) and feed (100%) before arriving at the farms, however, 40.5% of the farms used little or no disinfectants when washing the transport vehicles. Moreover, wild birds, and cats and dogs were well controlled on most of the farms (each 94.6%), but only 74.3% of farms offered rodent control programs. Also, only 27.0% of the farms used farm-specific shoes and clothing as well as footbath disinfection for entrance. These findings can be useful in developing policies and guidelines for sustainable and responsible broiler chicken production and reduction of antimicrobial use in Korea.
Key words: biosecurity, antimicrobial use, broiler, integrated operation
INTRODUCTION
Broilers are usually raised in intensive indoor production systems commonly used by large companies and an estimated 97.6% of chicken meat are also raised in intensive system of integrated broiler operations in Korea (EKAPE, 2022). However, the fast growth rate of intensively raised broilers leads to high mortality rate associated with health and welfare problems including metabolic issue, leg disorders, contact dermatitis, and low activity levels, high stocking density increases the risk of transmission of disease within flocks, and thermal stress can also cause intestinal injury (ASOA, 2017; EMA and EPSA, 2017; Baxter et al., 2020). Moreover, high levels of ammonia can also compromise the immune system of bird, leading to an increase in the incidence of the respiratory diseases (ASOA, 2017). Therefore, proper implementation of various external (e.g., control of transport vehicles, visitors, wild birds, and farm fence) and internal (e.g., disinfection and cleaning, biosecurity between poultry house) biosecurity practices are a fundamental step in preventing the spread of diseases (Gelaude et al., 2014). Caekebeke et al. (2020) reported that there were no disease outbreaks following implementation of high-level biosecurity in poultry farms and antimicrobial use was not necessary in healthy poultry.
But, birds under intensive production systems require more antimicrobial agents for therapeutic or prophylactic purposes (Agyare et al., 2018; Azabo et al., 2022). In particular, since antimicrobials in broilers are mainly administered to the whole flock, they may inappropriately be administrated to healthy or uninfected broilers, resulting in the presence of antimicrobial residues in the meat as well as the emergence of antimicrobial resistance (AMR) (Landoni and Albarellos, 2015). Moreover, Gerber et al. (2007) reported that, irrespective of dose, an estimated 75% of antimicrobial agents administered to intensively reared broilers may be excreted into the environment (Kümmerer, 2009; Wongsuvan et al., 2018). Ultimately, AMR is a global public health threat because inappropriate use of antimicrobials in food animals poses a potential threat as AMR can spread to human, limiting treatment options. Although integrated broiler operations that are systematically operated have their own biosecurity manual, the biosecurity level or compliance with regulations for each operation are not well known in Korea. Therefore, the objective of this study was to analysis the current adoption of biosecurity practices and trends in antimicrobial use in 5 major integrated broiler chicken operations, which account for 50.2% of chicken meat production in Korea.
MATERIALS AND METHODS
Study Design
A total of 74 commercial farms from 5 major integrated broiler operations were randomly selected to analyze the trends in biosecurity practices and antimicrobial use during 2021 in Korea. The numbers of commercial broiler farms surveyed by the 5 integrated broiler operations (A–E) was 15, 20, 15, 14, and 10 farms, respectively (Figure 1). A situational analysis of biosecurity practices and antimicrobial use during the broiler grow-out period was conducted using a questionnaire included: production environments, antimicrobials and disinfectants use, and biosecurity and management practices. The questionnaire was completed by the farm owners, and data were collected on the basis of their responses.
Figure 1.
Distribution of commercial farms by 5 integrated broiler operations (A–E). Farms were located across the country, and the concentration of color in the squares varies depending on the number of densely populated farms in each region.
Statistical Analysis
The Statistical Package for the Social Sciences (SPSS) v.26 (IBM Corp., Armonk, NY) was used for statistical analyses. The Pearson's chi-squared test with Bonferroni correction was performed. Differences were considered significant at P < 0.05.
RESULTS
Analysis of Production Environments
A situational analysis of the production environment of commercial farms by 5 integrated broiler operations is shown in Table 1. Among a total of 74 farms, farm types was significantly higher in organic-certified (66.2%) and HACCP-certified farms (50.0%) than conventional (23.0%) and animal welfare-certified (9.5%) farms (P < 0.05). Moreover, flock size per production cycle was significantly higher at 30,000 to 60,000 (43.2%) and 60,000 to 100,000 (37.8%) (P < 0.05), and most of the farms surveyed had only a few houses—68.9% had 1 to 4 houses. Most of the farms had windowless houses (86.5%), mechanical ventilation system (91.9%), and drinking water supply through groundwater (97.3%). The highest stocking density per 3.3 m2 (0.5 birds/ft2) was 66 to 70 birds (27.0%), followed by 56 to 60 birds (24.3%) and 61 to 65 birds (21.6%). Moreover, although 43 (58.1%) among 74 farms were using litter that was either new or used once, 10 (13.5%) farms were using litter reused more than 4 times. In particular, 6 (30.0%) and 4 (26.7%) farms in operations B and C, respectively, were only use litter more than 4 times. A period of downtime between flock and mortality during the first week were significantly higher within 20 d (50.0%) and 1 to 2% (45.9%), respectively (P < 0.05). Moreover, 96 to 98% (32.4%) and 98 to 100% (35.1%) livability were highest.
Table 1.
Situational analysis of production environments by 5 integrated broiler operations.
| Subgroup | No. of farms included by each integrated broiler operation (%) |
|||||
|---|---|---|---|---|---|---|
| A (n = 15)1 | B (n = 20) | C (n = 15) | D (n = 14) | E (n = 10) | Total (n = 74) | |
| Farm type | ||||||
| Conventional | 6 (40.0) | 2 (10.0) | 2 (13.3) | 5 (35.7) | 2 (20.0) | 17 (23.0)B |
| Organic | 7 (46.7)b | 18 (90.0)a | 8 (53.3)a,b | 9 (64.3)a,b | 7 (70.0)a,b | 49 (66.2)A |
| HACCP | 7 (46.7)a,b | 13 (65.0)a | 11 (73.3)a | 3 (21.4)b | 3 (30.0)b | 37 (50.0)A |
| Animal welfare | 1 (6.7)a,b | 0 (0.0)b | 6 (40.0)a | 0 (0.0)b | 0 (0.0)b | 7 (9.5)B |
| Number of birds (per cycle) | ||||||
| ≤30,000 | 1 (6.7) | 0 (0.0) | 0 (0.0) | 1 (7.1) | 1 (10.0) | 3 (4.1)B |
| 30,000< to ≤60,000 | 6 (40.0) | 13 (65.0) | 3 (20.0) | 6 (42.9) | 4 (40.0) | 32 (43.2)A |
| 60,000< to ≤100,000 | 8 (53.3) | 6 (30.0) | 6 (40.0) | 3 (21.4) | 5 (50.0) | 28 (37.8)A |
| >100,000 | 0 (0.0) | 1 (5.0) | 6 (40.0) | 4 (28.6) | 0 (0.0) | 11 (14.9)B |
| Number of houses | ||||||
| 1 | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 1 (10.0) | 1 (1.4)B |
| 2 | 4 (26.7) | 6 (30.0) | 2 (13.3) | 4 (28.6) | 2 (20.0) | 18 (24.3)A |
| 3 | 6 (40.0) | 5 (25.0) | 5 (33.3) | 1 (7.1) | 1 (10.0) | 18 (24.3)A |
| 4 | 2 (13.3) | 2 (10.0) | 4 (26.7) | 2 (14.3) | 4 (40.0) | 14 (18.9)A |
| >5 | 3 (20.0) | 7 (35.0) | 4 (26.7) | 7 (50.0) | 2 (20.0) | 23 (31.1)A |
| House system | ||||||
| Windowless house | 13 (86.7) | 19 (95.0) | 14 (93.3) | 11 (78.6) | 7 (70.0) | 64 (86.5)A |
| Windowed house | 2 (13.3) | 1 (5.0) | 1 (6.7) | 3 (21.4) | 3 (30.0) | 10 (13.5)B |
| Ventilation system | ||||||
| Natural | 2 (13.3) | 0 (0.0) | 0 (0.0) | 3 (21.4) | 1 (10.0) | 6 (8.1)B |
| Mechanical | 13 (86.7) | 20 (100.0) | 15 (100.0) | 11 (78.6) | 9 (90.0) | 68 (91.9)A |
| Water supply | ||||||
| Groundwater | 15 (100.0) | 20 (100.0) | 13 (86.7) | 14 (100.0) | 10 (100.0) | 72 (97.3)A |
| Waterworks | 0 (0.0) | 0 (0.0) | 2 (13.3) | 0 (0.0) | 0 (0.0) | 2 (2.7)B |
| Stocking density per 3.3 m2 | ||||||
| ≤50 | 1 (6.7) | 1 (5.0) | 1 (6.7) | 2 (14.3) | 1 (10.0) | 6 (8.1)A,B |
| 50< to ≤55 | 0 (0.0) | 3 (15.0) | 5 (33.3) | 0 (0.0) | 2 (20.0) | 10 (13.5)A,B |
| 55< to ≤60 | 2 (13.3)a,b | 7 (35.0)a,b | 0 (0.0)b | 4 (28.6)a,b | 5 (50.0)a | 18 (24.3)A |
| 60< to ≤65 | 2 (13.3) | 6 (30.0) | 4 (26.7) | 4 (28.6) | 0 (0.0) | 16 (21.6)A,B |
| 65< to ≤70 | 9 (60.0)a | 2 (10.0)b | 3 (20.0)a,b | 4 (28.6)a,b | 2 (20.0)a,b | 20 (27.0)A |
| >70 | 1 (6.7) | 1 (5.0) | 2 (13.3) | 0 (0.0) | 0 (0.0) | 4 (5.4)B |
| Number of times that the litter was reused | ||||||
| 0 | 0 (0.0) | 6 (30.0) | 0 (0.0) | 5 (35.7) | 1 (10.0) | 12 (16.2)B |
| 1 | 14 (93.3)a | 1 (5.0)b | 4 (26.7)a,b | 8 (57.1)a,b | 4 (40.0)a,b | 31 (41.9)A |
| 2 | 0 (0.0) | 1 (5.0) | 5 (33.3) | 1 (7.1) | 3 (30.0) | 10 (13.5)B |
| 3 | 1 (6.7) | 6 (30.0) | 2 (13.3) | 0 (0.0) | 2 (20.0) | 11 (14.9)B |
| ≥4 | 0 (0.0) | 6 (30.0) | 4 (26.7) | 0 (0.0) | 0 (0.0) | 10 (13.5)B |
| Downtime between flocks (d) | ||||||
| ≤20 | 12 (80.0)a | 6 (30.0)b | 9 (60.0)a,b | 4 (28.6)a,b | 6 (60.0)a,b | 37 (50.0)A |
| 20< to ≤24 | 3 (20.0) | 4 (20.0) | 3 (20.0) | 4 (28.6) | 3 (30.0) | 17 (23.0)B |
| >24 | 0 (0.0)b | 10 (50.0)a | 3 (20.0)a,b | 6 (42.9)a | 1 (10.0)a,b | 19 (25.7)B |
| Mortality during 1 wk of age (%) | ||||||
| ≤0.5 | 0 (0.0) | 2 (10.0) | 0 (0.0) | 1 (7.1) | 2 (20.0) | 5 (6.8)C |
| 0.5< to ≤1 | 2 (13.3) | 3 (15.0) | 3 (20.0) | 2 (14.3) | 3 (30.0) | 13 (17.6)B |
| 1< to ≤2 | 8 (53.3) | 7 (35.0) | 4 (26.7) | 11 (78.6) | 4 (40.0) | 34 (45.9)A |
| >2 | 5 (33.3) | 8 (40.0) | 8 (53.3) | 0 (0.0) | 1 (10.0) | 22 (29.7)A,B |
| Livability (%) | ||||||
| ≤96 | 2 (13.3) | 6 (30.0) | 4 (26.7) | 0 (0.0) | 0 (0.0) | 12 (16.2) |
| 96< to ≤98 | 9 (60.0)a | 3 (15.0)a,b | 10 (66.7)a | 2 (14.3)a,b | 0 (0.0)b | 24 (32.4) |
| 98< to ≤100 | 2 (13.3)a,b | 5 (25.0)a,b | 1 (6.7)b | 12 (85.7)a | 6 (60.0)a,b | 26 (35.1) |
| >100 | 2 (13.3) | 6 (30.0) | 0 (0.0) | 0 (0.0) | 4 (40.0) | 12 (16.2) |
n = No. of farms included in each operation.
Values with different lowercase superscript letters represent significant difference among operations, while different uppercase superscript letters represent significant differences between total response subgroup (P < 0.05).
Distribution of Antimicrobial Prescribing Frequency
The distribution of antimicrobial prescribing frequency throughout the growing period by 5 integrated broiler operations is shown in Table 2. The highest prescribing frequency was 2 times (39.2%), followed by 1 (25.7%) and 3 (25.7%) times. Only 3 (4.1%) among 74 farms were not prescribed antimicrobials.
Table 2.
Antimicrobial prescribing frequency throughout the growing period by 5 integrated broiler operations.
| Frequency1 | No. of farms included by each integrated broiler operation (%) |
|||||
|---|---|---|---|---|---|---|
| A (n = 15) | B (n = 20) | C (n = 15) | D (n = 14) | E (n = 10) | Total (n = 74) | |
| 0 | 0 (0.0) | 0 (0.0) | 1 (6.7) | 0 (0.0) | 2 (20.0) | 3 (4.1)B |
| 1 | 1 (6.7) | 8 (40.0) | 5 (33.3) | 3 (21.4) | 2 (20.0) | 19 (25.7)A |
| 2 | 9 (60.0) | 6 (30.0) | 3 (20.0) | 6 (42.9) | 5 (50.0) | 29 (39.2)A |
| 3 | 5 (33.3) | 4 (20.0) | 4 (26.7) | 4 (28.6) | 1 (10.0) | 19 (25.7)A |
| 4 | 0 (0.0) | 2 (10.0) | 2 (13.3) | 1 (7.1) | 0 (0.0) | 4 (5.4)B |
No. of times antimicrobials were prescribed.
Values with different uppercase superscript letters represent significant difference in total, but there were no significant differences between operations by antimicrobial prescribing frequency (P < 0.05).
Analysis of Antimicrobial use
Comparative analysis of antimicrobial use throughout the growing period is shown in Table 3. Overall, β-lactams (45.3%) were the most commonly prescribed antimicrobial class, followed by phenicols (24.7%), fluoroquinolones (16.0%), macrolides (8.7%), and tetracyclines (1.3%) (P < 0.05). However, phenicols and fluoroquinolones were significantly highly prescribed in farms of operation C, and operations D and E, respectively (P < 0.05). The most prevalence age for antimicrobial prescription was the highest in 15 to 22-days old (42.7%), followed by 6-days old or less (31.3%). The antimicrobials were used more for prevention (70.7%) than for treatment (29.3%) of disease, and via drinking water (100%). Also, most of the antimicrobials were recommended by a veterinarian (80.7%) and purchased from a veterinary hospital (78.0%). But susceptibility testing to antimicrobials has not been performed on most farms (91.3%).
Table 3.
Comparative analysis of antimicrobial use throughout the growing period by 5 integrated broiler operations.
| Subgroup | No. of prescriptions for antimicrobials by each integrated broiler operation (%) |
|||||
|---|---|---|---|---|---|---|
| A (n = 34) | B (n = 40) | C (n = 30) | D (n = 31) | E (n = 15) | Total (n = 150) | |
| Antimicrobial class | ||||||
| β-Lactams | 16 (47.1) | 19 (47.5) | 13 (43.3) | 13 (41.9) | 7 (46.7) | 68 (45.3)A |
| Phenicols | 10 (29.4)a,b | 10 (25.0)a,b | 14 (46.7)a | 2 (6.5)b | 1 (6.7)a,b | 37 (24.7)A,B |
| Fluoroquinolones | 1 (2.9)b | 8 (20.0)a,b | 0 (0.0)b | 10 (32.3)a | 5 (33.3)a | 24 (16.0)B |
| Macrolides | 1 (2.9) | 3 (7.5) | 2 (6.7) | 6 (19.4) | 1 (6.7) | 13 (8.7)B,C |
| Tetracyclines | 2 (5.9) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 2 (1.3)C |
| Other | 4 (11.8) | 0 (0.0) | 1 (3.3) | 0 (0.0) | 1 (6.7) | 6 (4.0)C |
| Age (d) of chicken that antimicrobials were administered | ||||||
| ≤6 | 10 (29.4) | 10 (25.0) | 8 (26.7) | 12 (38.7) | 7 (46.7) | 47 (31.3)A,B |
| 6< to ≤14 | 10 (29.4) | 8 (20.0) | 7 (23.3) | 7 (22.6) | 3 (20.0) | 35 (23.3)B |
| 14< to ≤22 | 14 (41.2) | 21 (52.5) | 15 (50.0) | 9 (29.0) | 5 (33.3) | 64 (42.7)A |
| >22 | 0 (0.0) | 1 (2.5) | 0 (0.0) | 3 (9.7) | 0 (0.0) | 4 (2.7)C |
| Reason | ||||||
| Treatment | 4 (11.8) | 14 (35.0) | 12 (40.0) | 8 (25.8) | 6 (40.0) | 44 (29.3)B |
| Prevention | 30 (88.2) | 26 (65.0) | 18 (60.0) | 23 (74.2) | 9 (60.0) | 106 (70.7)A |
| Route | ||||||
| Feed | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0)B |
| Water | 34 (100.0) | 40 (100.0) | 30 (100.0) | 31 (100.0) | 15 (100.0) | 150 (100.0)A |
| Injection | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0)B |
| Where to buy | ||||||
| Pharmaceutical company | 3 (8.8)b | 0 (0.0)b | 7 (23.3)a,b | 16 (51.6)a | 4 (26.7)a,b | 30 (20.0)B |
| Veterinary hospital | 31 (91.2)a,b | 40 (100.0)a | 23 (76.7)a,b | 14 (45.2)b | 9 (60.0)a,b | 117 (78.0)A |
| Veterinary pharmacy | 0 (0.0) | 0 (0.0) | 0 (0.0) | 1 (3.2) | 2 (13.3) | 3 (2.0)C |
| Who recommended | ||||||
| Veterinarian | 31 (91.2)a,b | 40 (100.0)a | 19 (63.3)b | 22 (71.0)b | 9 (60.0)b | 121 (80.7)A |
| Pharmacy owner | 3 (8.8)a,b | 0 (0.0)b | 4 (13.3)a,b | 9 (29.0)a | 5 (33.3)a | 21 (14.0)B |
| Farm owner | 0 (0.0) | 0 (0.0) | 5 (16.7) | 0 (0.0) | 1 (6.7) | 6 (4.0)C |
| Other | 0 (0.0) | 0 (0.0) | 2 (6.7) | 0 (0.0) | 0 (0.0) | 2 (1.3)C |
| Performance of susceptibility test | ||||||
| Yes | 0 (0.0)b | 0 (0.0)b | 3 (10.0)a,b | 8 (25.8)a | 2 (13.3)a,b | 13 (8.7)B |
| No | 34 (100.0)a | 40 (100.0)a | 27 (90.0)a,b | 23 (74.2)b | 13 (86.7)a,b | 137 (91.3)A |
Values with different lowercase superscript letters represent significant differences among operations, while different uppercase superscript letters represent significant differences between total response subgroup (P < 0.05).
Analysis of Disinfectant use
Comparative analysis of disinfectant use throughout the growing period is shown in Table 4. Footbath disinfectant (64.9%) and spraying outside the poultry house (83.8%) were performed on many farms, but the use of quicklime (36.5%) and drinking water disinfectant (18.9%) was not common in farms. Interestingly, farms that were not disinfected during downtime between flock had a significantly highest prevalence (82.4%) (P < 0.05), moreover, farms from operations A, C, and D did not disinfect at all.
Table 4.
Comparative analysis of disinfectant use throughout the growing period by 5 integrated broiler operations.
| Subgroup | No. of farms included by each integrated broiler operation (%) |
|||||
|---|---|---|---|---|---|---|
| A (n = 15) | B (n = 20) | C (n = 15) | D (n = 14) | E (n = 10) | Total (n = 74) | |
| Footbath disinfection | ||||||
| Yes | 15 (100.0)a | 4 (20.0)b | 8 (53.3)a,b | 13 (92.9)a,b | 8 (80.0)a,b | 48 (64.9)A |
| No | 0 (0.0)b | 16 (80.0)a | 7 (46.7)a,b | 1 (7.1)a,b | 2 (20.0)a,b | 26 (35.1)B |
| Spray disinfection outside the poultry house | ||||||
| Yes | 14 (93.3) | 16 (80.0) | 13 (86.7) | 9 (64.3) | 10 (100.0) | 62 (83.8)A |
| No | 1 (6.7) | 4 (20.0) | 2 (13.3) | 5 (35.7) | 0 (0.0) | 12 (16.2)B |
| Use of quicklime (CaO) | ||||||
| Yes | 10 (66.7)a | 0 (0.0)b | 4 (26.7)a,b | 9 (64.3)a | 4 (40.0)a | 27 (36.5)B |
| No | 5 (33.3)b | 20 (100.0)a | 11 (73.3)a,b | 5 (35.7)b | 6 (60.0)a,b | 47 (63.5)A |
| Disinfection in drinking water | ||||||
| Yes | 0 (0.0)b | 12 (60.0)a | 1 (6.7)b | 0 (0.0)b | 1 (10.0)a,b | 14 (18.9)B |
| No | 15 (100.0)a | 8 (40.0)b | 14 (93.3)a | 14 (100.0)a | 9 (90.0)a | 60 (81.1)A |
| Disinfection between flocks | ||||||
| Never | 15 (100.0)a | 10 (50.0)b | 15 (100.0)a | 14 (100.0)a | 7 (70.0)a,b | 61 (82.4)A |
| Disinfection of water pipe lines | 0 (0.0) | 2 (10.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 2 (2.7)B |
| Spray disinfection inside the poultry house | 0 (0.0) | 8 (40.0) | 0 (0.0) | 0 (0.0) | 1 (10.0) | 9 (12.2)B |
| Fumigation of poultry houses | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 2 (20.0) | 2 (2.7)B |
Values with different lowercase superscript letters represent significant differences among operations, while different uppercase superscript letters represent significant differences between total response subgroup (P < 0.05).
Analysis of Biosecurity Practices
Comparative analysis of vehicles management throughout the growing period is shown in Table 5. The prevalence of farms that the same vehicle was used in several farms, but the vehicle washed before arriving at the farm, was most common (87.8%). However, 2 (14.3%) among 14 farms in operation D used vehicles without any restrictions. Most of the vehicles used to transport poultry were washed after one use (95.9%), but the prevalence of farms that always used a disinfectant when washing poultry transport vehicles was 59.5%. In particular, 18 (90.0%) of the 20 farms in operation B did not use disinfectants or did not know about them. Also, most farms tested transport vehicles to ensure that they were completely dry before poultry transport (94.6%), moreover, all feed transport vehicles could visit several farms, but were cleaned before arriving at the farms (100%).
Table 5.
Comparative analysis of vehicles management throughout the growing period by 5 integrated broiler operations.
| Subgroup | No. of farms included by each integrated broiler operation (%) |
|||||
|---|---|---|---|---|---|---|
| A (n = 15) | B (n = 20) | C (n = 15) | D (n = 14) | E (n = 10) | Total (n = 74) | |
| Transport vehicle control | ||||||
| Use without restrictions | 0 (0.0) | 0 (0.0) | 0 (0.0) | 2 (14.3) | 0 (0.0) | 2 (2.7)B |
| Several farms used the same vehicles, but wash the vehicles before arriving at the farm | 14 (93.3)a | 20 (100.0)a | 15 (100.0)a | 6 (42.9)b | 10 (100.0)a | 65 (87.8)A |
| Use of a farm vehicle | 1 (6.7)b | 0 (0.0)b | 0 (0.0)b | 6 (42.9)a | 0 (0.0)b | 7 (9.5)B |
| Wash cycles for poultry transport vehicles | ||||||
| Always | 15 (100.0) | 20 (100.0) | 13 (86.7) | 14 (100.0) | 9 (90.0) | 71 (95.9)A |
| Little or no | 0 (0.0) | 0 (0.0) | 2 (13.3) | 0 (0.0) | 1 (10.0) | 3 (4.1) B |
| Whether or not disinfectants were used when washing poultry transport vehicles | ||||||
| Always | 15 (100.0)a | 2 (10.0)b | 9 (60.0)a | 11 (78.6)a | 7 (70.0)a | 44 (59.5)A |
| Little or no | 0 (0.0)b | 18 (90.0)a | 6 (40.0)b | 3 (21.4)b | 3 (30.0)b | 30 (40.5)B |
| Drying after washing for poultry transport vehicles | ||||||
| Yes | 14 (93.3) | 20 (100.0) | 14 (93.3) | 14 (100.0) | 8 (80.0) | 70 (94.6)A |
| No | 1 (6.7) | 0 (0.0) | 1 (6.7) | 0 (0.0) | 2 (20.0) | 4 (5.4)B |
| Implementation of biosecurity for feed transport vehicles | ||||||
| No regulation | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0)B |
| Several farms use the same vehicles but wash the vehicles before arriving at the farm | 15 (100.0) | 20 (100.0) | 15 (100.0) | 14 (100.0) | 10 (100.0) | 74 (100.0)A |
| Feeding from the outside without access to the inside of the houses | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0)B |
Values with different lowercase superscript letters represent significant differences among operations, while different uppercase superscript letters represent significant differences between total response subgroup (P < 0.05).
Comparative analysis of carcass disposal and outdoor access management throughout the growing period are shown in Table 6. Carcass disposal was primarily carried out on farms (82.4%), most of which were fenced (79.7%) and used traps to control rodents (74.3%) and which were not accessible to wild birds (94.6%) and dogs/cats (94.6%). Thirty-eight (51.4%) farms received regular advice and biosecurity training from veterinarians, and 48.6% received occasional advice. Also, it was common to use only a disinfectant footbath at the entrance (58.1%) when entering and leaving individual houses, but 27.0% changed shoes and clothing by farm along with the footbath. Moreover, farms divided into clean and dirty area, which were always strictly enforced, was 63.5%.
Table 6.
Comparative analysis of carcass disposal and outdoor access management throughout the growing period by 5 integrated broiler operations,
| Subgroup | No. of farms included by each integrated broiler operation (%) |
|||||
|---|---|---|---|---|---|---|
| A (n = 15) | B (n = 20) | C (n = 15) | D (n = 14) | E (n = 10) | Total (n = 74) | |
| Disposal of dead chickens | ||||||
| Processing outside the farm | 9 (60.0)a | 0 (0.0)b | 1 (6.7)b | 2 (14.3)a,b | 1 (10.0)a,b | 13 (17.6)B |
| Processing inside the farm | 6 (40.0)b | 20 (100.0)a | 14 (93.3)a | 12 (85.7)a,b | 9 (90.0)a,b | 61 (82.4)A |
| Carcass collection cycle from outside | ||||||
| ≤7 | 8 (53.3)a | 0 (0.0)b | 1 (6.7)a,b | 2 (14.3)a,b | 0 (0.0)b | 11 (14.9)B |
| >7 | 1 (6.7) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 1 (10.0) | 2 (2.7)C |
| On farm | 6 (40.0)b | 20 (100.0)a | 14 (93.3)a | 12 (85.7)a,b | 9 (90.0)a,b | 61 (82.4)A |
| Farm fence | ||||||
| Yes | 10 (66.7) | 16 (80.0) | 11 (73.3) | 13 (92.9) | 9 (90.0) | 59 (79.7)A |
| No | 5 (33.3) | 4 (20.0) | 4 (26.7) | 1 (7.1) | 1 (10.0) | 15 (20.3)B |
| Rodent control programs present on the farm | ||||||
| Yes | 15 (100.0)a | 6 (30.0)b | 11 (73.3)a,b | 14 (100.0)a | 9 (90.0)a | 55 (74.3)A |
| No | 0 (0.0)b | 14 (70.0)a | 4 (26.7)a,b | 0 (0.0)b | 1 (10.0)b | 19 (25.7)B |
| Accessibility to wild birds | ||||||
| Yes | 0 (0.0) | 1 (5.0) | 0 (0.0) | 0 (0.0) | 3 (30.0) | 4 (5.4)B |
| No | 15 (100.0) | 19 (95.0) | 15 (100.0) | 14 (100.0) | 7 (70.0) | 70 (94.6)A |
| Accessibility to cats and dogs | ||||||
| Yes | 0 (0.0) | 1 (5.0) | 1 (6.7) | 0 (0.0) | 2 (20.0) | 4 (5.4)B |
| No | 15 (100.0) | 19 (95.0) | 14 (93.3) | 14 (100.0) | 8 (80.0) | 70 (94.6)A |
| Regular visits and advice from poultry veterinarians | ||||||
| Receive regular advice and biosecurity trainings | 13 (86.7)a | 2 (10.0)b | 8 (53.3)a,b | 11 (78.6)a | 4 (40.0)a,b | 38 (51.4)A |
| Sometimes | 2 (13.3)b | 18 (90.0)a | 7 (46.7)b | 3 (21.4)b | 6 (60.0)a,b | 36 (48.6)A |
| Never | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0)B |
| Biosecurity between poultry houses | ||||||
| No | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0)C |
| Entrance: only disinfectant foot bath | 2 (13.3)b | 20 (100.0)a | 9 (60.0)b | 7 (50.0)b | 5 (50.0)b | 43 (58.1)A |
| Entrance: farm-specific shoes and clothing changes | 6 (40.0)a | 0 (0.0)b | 2 (13.3)a,b | 2 (14.3)a,b | 1 (10.0)a,b | 11 (14.9)B |
| Entrance: disinfectant foot bath, farm-specific shoes, and clothing changes | 7 (46.7)a | 0 (0.0)b | 4 (26.7)a,b | 5 (35.7)a | 4 (40.0)a | 20 (27.0)B |
| Farm entrance | ||||||
| Direct access to the farm without distinction between clean and dirty areas | 0 (0.0) | 0 (0.0) | 1 (6.7) | 0 (0.0) | 0 (0.0) | 1 (1.4)C |
| Divided into clean and dirty areas, but not always strictly enforced | 3 (20.0)b | 18 (90.0)a | 1 (6.7)b | 2 (14.3)b | 2 (20.0)b | 26 (35.1)B |
| Divided into clean and dirty areas, always strictly enforced | 12 (80.0)a | 2 (10.0)b | 13 (86.7)a | 12 (85.7)a | 8 (80.0)a | 47 (63.5)A |
Values with different lowercase superscript letters represent significant differences among operations, while different uppercase superscript letters represent significant differences between total response subgroup (P < 0.05).
A comparative analysis of personnel management throughout the growing period is shown in Table 7. The prevalence of farms with restricted access for visitors, including veterinarians, had 62.2%, and 24.3% of the farms did not allow visitors at all. Although farmworkers were often trained through farm biosecurity manuals, 51.4% of the farms did not place biosecurity manuals in hazardous areas. In addition, most of the farms did not employ foreign farmworkers (85.1%), and farmworkers in all farms responded that they had no opportunities to contact outside chickens (100%).
Table 7.
Comparative analysis of personnel management throughout the growing period by 5 integrated broiler operations.
| Subgroup | No. of farms included by each integrated broiler operation (%) |
|||||
|---|---|---|---|---|---|---|
| A (n = 15) | B (n = 20) | C (n = 15) | D (n = 14) | E (n = 10) | Total (n = 74) | |
| Farm access rule for visitors (including veterinarians) | ||||||
| Yes | 6 (40.0) | 12 (60.0) | 11 (73.3) | 10 (71.4) | 7 (70.0) | 46 (62.2)A |
| No | 0 (0.0) | 8 (40.0) | 0 (0.0) | 2 (14.3) | 0 (0.0) | 10 (13.5)B |
| Not allowed | 9 (60.0)a | 0 (0.0)b | 4 (26.7)a,b | 2 (14.3)a,b | 3 (30.0)a,b | 18 (24.3)B |
| Possession of farm biosecurity manual | ||||||
| No farm biosecurity manual and farmworker training | 0 (0.0) | 5 (25.0) | 3 (20.0) | 1 (7.1) | 0 (0.0) | 9 (12.2)B |
| Farmworkers are often trained through farm biosecurity manuals, but is not placed in hazardous areas | 8 (53.3)a,b | 14 (70.0)a,b | 4 (26.7)b | 3 (21.4)b | 9 (90.0)a | 38 (51.4)A |
| Farmworker training is conducted through the farm biosecurity manual, and it is placed in a hazardous area so that employees can check it | 7 (46.7)a,b | 1 (5.0)b | 8 (53.3)a,b | 10 (71.4)a | 1 (10.0)b | 27 (36.5)A |
| Foreign farmworker | ||||||
| Yes | 2 (13.3) | 0 (0.0) | 5 (33.3) | 2 (14.3) | 2 (20.0) | 11 (14.9)B |
| No | 13 (86.7) | 20 (100.0) | 10 (66.7) | 12 (85.7) | 8 (80.0) | 63 (85.1)A |
| Opportunities for farmworkers to have contact with outside chickens | ||||||
| Yes | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0)B |
| No | 15 (100.0) | 20 (100.0) | 15 (100.0) | 14 (100.0) | 10 (100.0) | 74 (100.0)A |
Values with different lowercase superscript letters represent significant differences among operations, while different uppercase superscript letters represent significant differences between total response subgroup (P < 0.05).
DISCUSSION
Biosecurity is a major practice to prevent the spread of disease and introduction of new infections in poultry and includes reducing the risk of people, animals, equipment, and vehicles bringing infectious disease onto farms. The broiler chicken industry is predominantly vertically integrated, with company ownership of breeding farms, multiplication farms, hatcheries, feed mills, some broiler growing farms, and processing plants. This study aimed to analyze of biosecurity practices and antimicrobial use during the broiler grow-out period by 5 integrated broiler operations in Korea, and 66.2% of the participating farms confirmed as organic-certified. Guarino Amato and Castellini (2022) reported that the organic broiler production system operated according to precise and specific production standards are increasing worldwide. Moreover, demand for organic poultry products, a production system that reduces chemical use and emphasis on animal welfare, has increased as it is perceived to be safer and more nutritious than conventionally raised poultry (Cobanoglu et al., 2014; Niggli, 2015). Therefore, the organic-certified broiler production in Korea is also increasing quickly and is expected to continue to grow (MAFRA, 2020).
Previous studies have reported that farms with lower animal density reduce the burden of AMR bacteria (Pesciaroli et al., 2020; Massaccesi et al., 2021). Tsiouris et al. (2015) also reported that increased stocking densities in broiler production generally result in higher economic returns in the production cycle, but higher stocking densities also increase mortality due to bird stress and rapid horizontal spread of pathogens. In this study, 66.7 and 33.3% of farms in operations A and C revealed the highest stocking densities, with more than 65 birds per 3.3 m2, and the livability of 98% or less was 73.3 and 93.4%, respectively, lower than other operations.
A windowless house and mechanical ventilation system maintains proper temperature, humidity, and aeration, removes harmful gases from inside, and has many benefits for animal welfare and production efficiency. This study also observed that broiler farms were equipped with modern facilities, including windowless houses (86.5%) and mechanical ventilation systems (91.9%).
Chuppava et al. (2019) reported that broiler manure is a major reservoir of AMR bacteria, and reuse of litter containing this manure could have a significant impact on the persistence of AMR bacteria on a farm. In this study, although 16.2% of farms did not reuse litter, the significantly higher percentage (41.9%) of farms reused litter only once. However, it was revealed that 60.0 and 40.0% of farms in operations B and C, respectively, reused litter 3 or more times. Although it has not been confirmed that the use of antimicrobials in these farms is higher than that in other farms, further investigations are needed to determine the relationship between the number of times litter is reused, the occurrence of diseases, and the use of antimicrobials.
In this study, antimicrobial prescribing frequency during the broiler grow-out period was 25.7, 39.2, and 25.7% for once, twice, and 3 times, respectively, and there were no significant differences among operations. Antimicrobials were significantly highly administered at 15 to 22 d of age (42.7%), and most antimicrobials were observed to be used prior to 22 d of age (97.3%) due to withdrawal periods ranging from 1 or 2 d to a couple of weeks. Moreover, β-lactams (45.3%) were used significantly higher, probably because ampicillin was continued to be administered to prevent necrotic enteritis caused by intestinal overgrowth of Clostridium perfringens, which usually coincides with coccidiosis at 2 to 5 wk of age. Also, phenicols, fluoroquinolones, and macrolides were prescribed on 24.7, 16.0, and 8.7% of farms, respectively. The administration of florfenicol of the phenicols, and enrofloxacin of the fluoroquinolones, has been widely used for the prevention or treatment of colibacillosis caused by Escherichia coli, and tilmicosin of the macrolides has been used for respiratory disease caused by Mycoplasma spp. in Korea. Although enrofloxacin was prohibited from being used in poultry since 2021 in Korea, it is estimated that the remaining enrofloxacin owned by the farms was administered in 2022.
In this study, antimicrobials were administered primarily by the drinking water route (100%) for prophylaxis (70.7%). Administration through drinking water is the preferred management method because it is convenient and economical to treat and prevent the flock, and diseased birds may continue drinking even if they stop eating (Landoni and Albarellos, 2015). This administration route also allows healthy birds to consume more water and is a preventative approach to control the spread of bacteria from diseased birds to healthy birds (Gray et al., 2021). Moreover, in this study, antimicrobials were purchased from veterinary hospitals (78.0%) on the recommendation of veterinarians (80.7%). Caneschi et al. (2023) reported that antimicrobials should be used under the advice of a veterinarian, as it prevents the development of AMR due to misuse of antimicrobials and enables effective antibiotic use. Therefore, veterinarians need to use antimicrobials responsibly, including accurate disease diagnosis and prescribing only necessary antimicrobials. But, 91.3% of farms did not perform susceptibility testing. Macrolides, fluoroquinolones and third- and higher-generation cephalosporins are classified as “critically important and highest priority for human medicine” by the World Health Organization (WHO, 2019), therefore, these classes should be used in food production animals after antimicrobial susceptibility testing.
In this study, several biosecurity practices have been identified as risk factors for the transmission of pathogens. ELSaidy et al. (2015) reported that birds consume about 1.6 to 2.0 times as much water as feed by weight, therefore, drinking water disinfection is important in preventing the spread of disease through drinking water on farms. In this study, farms that did not disinfection in water pipe lines after depletion were significantly higher (97.3%). Also, farms that did not disinfection of inside and fumigation after depletion were 87.8 and 97.3%, respectively. Mo et al. (2016) reported that the probability of being positive for cephalosporin-resistant E. coli in environments of poultry houses was approximately 13 times higher when the previous flock was cephalosporin-resistant E. coli-positive than when the previous flock was cephalosporin-resistant E. coli-negative. Therefore, sufficient disinfection after depletion is essential for preventing the spread of pathogenic as well as resistant bacteria and further reduction of the frequency of antimicrobial use.
The use of farm vehicles exclusive for each farm for poultry transportation and feeding is the best practice, but if this is not possible, it is recommended that transport vehicles be disinfected prior to arrival at the farm to prevent the introduction of pathogens from farm to farm (Van Limbergen et al., 2018). In this study, vehicles for poultry transport (87.8%) and for feeding (100%) are washed before arriving at the farm, however, 40.5% of farms used little or no disinfectants when washing transport vehicles. Previous studies have reported that continuous contact of contaminated transport vehicles with other farms significantly increases the risk of diseases transmission (Hege et al., 2022; Gelaude et al., 2014; Tanquilut et al., 2020). Therefore, the use of disinfectants should be continually promoted to eliminate disease-causing agents in transport vehicles.
Dead chickens are a potential source of infection and should be collected immediately and stored in a designated, well-insulated area, preferably equipped with cooling facilities, to prevent the spread of pathogens (Gelaude et al., 2014; Tanquilut et al., 2020). Additionally, pathogens can be introduced into farms by rodents, wild birds, and pet animals, thus, a farm fence should be installed to minimize contact between these animals and poultry. In particular, rodents can play a significant role in transmitting pathogens, either as mechanical or biological vectors (Domanska-Blicharz et al., 2023). In this study, wild birds, and cats and dogs were well controlled from farms (each 94.6%) by 5 integrated operations, but rodent control programs need to be improved.
Humans can also be mechanical vectors for the transmission of various pathogens (Tanquilut et al., 2020). According to a study conducted in the Netherlands, it was found that the highest transmission route for external pathogens was not wearing specific work clothing prior to entering the poultry house (Ssematimba et al., 2013). Interestingly, farms that disinfected only footbath (58.1%) were significantly higher in this study. Therefore, it is necessary to encourage the use of farm-specific shoes and clothing as well as footbath disinfection before entering the poultry house to reduce the risk of transmission of pathogens through humans. Also, biosecurity measures should be continually implemented for visitors, and it is recommended to limit their access and keep them as far away from poultry houses as possible. The findings of this study can be useful in developing policies and guidelines for sustainable and responsible broiler chicken production and reduction of antimicrobial use in Korea.
ACKNOWLEDGMENTS
This work was supported by the Animal and Plant Quarantine Agency, Ministry of Agriculture, Food and Rural affairs, Republic of Korea (Grant Number Z-1543061-2021-23-02).
DISCLOSURES
The authors declare that they have no competing interest.
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