Quantitative Risk Evaluation of Antimicrobial-Resistant Vibrio parahaemolyticus Isolated from Farmed Grey Mullets in Singapore
Abstract
:1. Introduction
2. Methodology
2.1. Collection of Survey Data for Exposure Assessment
2.2. Sample Collection
2.2.1. Sampling Period
2.2.2. Farm and Retail Sampling
2.2.3. Sample Processing
2.2.4. Direct Plate Count of Presumptive Vibrio Species
2.2.5. Phenotypic Identification of Haemolytic Strains
2.2.6. 16 s rRNA Gene Amplification and Sequencing
2.2.7. Antimicrobial Susceptibility Testing
2.3. Quantitative Risk Evaluation Model Framework
- Grey mullets harvested from the farm were not processed but were quickly packed in ice and sent to the fishery port and subsequently the hypermarket. Once at the hypermarket, they were placed on open-air fish ice beds for display. Processing of the food fish were carried out at the consumer’s home.
- The survivability fitness of different V. parahaemolyticus strains was considered equal.
- Within the ARRA framework for a specified antimicrobial resistance, co- and cross-resistance traits of V. parahaemolyticus strains regarding the other two antimicrobials were not considered.
- Only direct exposure from the consumption of contaminated seafood to consumers was considered. Secondary transmission of infection, including transmission through workers within the food chain, was not considered.
- Human host immunity to infection from V. parahaemolyticus was not considered.
2.3.1. Hazard Identification
2.3.2. Exposure Assessment
V. parahaemolyticus Growth Rate Modelling and Adjustment Factors
- The growth rate of haemolytic of V. parahaemolyticus were the same across all strains considered.
- The lag phase associated during the harvest stage was considered negligible, as there was no change in the growth environment.
- The growth pattern of haemolytic V. parahaemolyticus exhibited in grey mullet are highly similar to that in mackerel, as both share highly similar biological traits.
Concentration and Occurrence of Haemolytic V. parahaemolyticus at Pre-Harvest and Retail
Harvesting Conditions and Transportation to Hypermarket
Retail Display and Transportation to Home
Preparation, Cooking and Consumption Patterns
2.3.3. Hazard Characterisation
Dose-Response Relationship
2.3.4. Risk Characterisation
3. Results
3.1. Occurrence and Concentration of Haemolytic, Ampicillin-Resistant, Penicillin G-Resistant and Tetracycline-Resistant Vibrio parahaemolyticus
3.2. Comparison of Risk Characterisation Outputs across Scenarios
3.3. Sensitivity Analysis
4. Discussion
4.1. Occurrence and Concentration Trends of Vibrio parahaemolyticus in Grey Mullet
4.2. Comparison of ARRA Risk Estimates to Other Studies
4.3. Comparison among ARRAs
4.4. Exposure Risk Estimates, Sensitivity Analysis of Intervention Measures and Limitations of Study
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Symbol | Description | Equation | References |
---|---|---|---|
Exposure assessment | |||
Growth rate equations | |||
Growth rate in broth model (Log10/min) | [27] | ||
Growth rate adjustment (Log10/h) | [28,29] | ||
Initial occurrence and concentration equations | |||
Occurrence of haemolytic Vp | RiskBeta (positives + 1, negatives + 1) | Author’s input | |
# | Total concentration of Vp in fish body (Log10/g) | [28,30] | |
Growth during harvest | |||
Harvest time (h) | RiskTriang (1, 1.5, 2) | Author’s input | |
Harvest temperature (K) | RiskPert (299.05, 301.55, 305.45) | [31] | |
Concentration of Vp (Log10/g) | - | ||
Growth during transport to retail | |||
Transport time (h) | RiskUniform (13.5, 14.5) | Author’s input | |
Transport temperature (K) | RiskPert (276.15, 279.15, 282.15) | [28] | |
Concentration of Vp (Log10/g) | - | ||
Growth during retail display | |||
Display time for majority of purchases (h) | RiskUniform (0.5, 3.5) | Author’s input | |
Display time for remaining purchases (h) | RiskPert (3.5, 5.5, 12.5) | Author’s input | |
Overall display time (h) | Author’s input | ||
Display temperature (K) | RiskPert (278.15, 283.15, 288.15) | [32] | |
Concentration of Vp (Log10/g) | - | ||
Growth during transport to home | |||
Transport time (h) | RiskTriang (0.25, 0.5, 0.75) | [32] | |
Transport temperature (K) | RiskPert (299.05, 301.55, 305.45) | [31] | |
Concentration of Vp (Log10/g) | - | ||
Preparation and cooking | |||
Fish body cavity, washing scenario (Log10/g) | RiskNormal (−1.9921, 0.4545) | [33] | |
Fish body cavity, no washing scenario (Log10/g) | RiskNormal (−0.8449, 0.4897) | [33] | |
Overall washing scenario (Log10/g) | Prepwash—90% Prepno wash—10% | Author’s input | |
Heat inactivation (Log10/g) | RiskUniform (−1.1, −7) | [34] | |
& | Concentration of Vp (Log10/g) | - | |
Concentration of Vp (Log10/g) | - | ||
Serving Size (grams) | RiskTriang (0, 61.2, 197.3) | [35] | |
Dose (CFU) | - | ||
Hazard characterisation | |||
Beta Poisson dose-response | [29] | ||
@ | Occurrence change from farm to retail | - | |
Probability of illness per serving | @ | - | |
Risk characterisation | |||
Singapore’s population | 5,703,569 | [36] | |
Population proportion consuming finfish | 0.92 | [37] | |
Population proportion consuming grey mullet | Author’s input | ||
Exposed population | - | ||
Number of meals per week | RiskNormal (10.37, 7.586) | [37] | |
Probability of illness per person per year | - | ||
Cases per year | - |
FDA Model | α | β | Probability Weight |
---|---|---|---|
1 | 1.47 × 106 | 3.53 × 1014 | 3.40 × 10−4 |
2 | 1.26 × 107 | 7.20 × 1014 | 4.12 × 10−3 |
3 | 6.37 × 102 | 1.65 × 1010 | 2.06 × 10−2 |
4 | 3.58 × 101 | 5.42 × 108 | 5.49 × 10−2 |
5 | 2.08 × 101 | 1.99 × 108 | 8.23 × 10−2 |
6 | 1.49 × 101 | 8.78 × 107 | 6.58 × 10−2 |
7 | 1.06 × 101 | 2.99 × 107 | 2.20 × 10−2 |
8 | 3.89 | 2.28 × 108 | 6.90 × 10−4 |
9 | 1.31 | 2.93 × 107 | 8.23 × 10−3 |
10 | 5.20 × 10−1 | 3.61 × 106 | 4.12 × 10−2 |
11 | 4.70 × 10−1 | 1.50 × 106 | 1.10 × 10−1 |
12 | 6.00 × 10−1 | 1.31 × 106 | 1.65 × 10−1 |
13 | 1.00 | 1.80 × 106 | 1.32 × 10−1 |
14 | 8.59 | 1.30 × 107 | 4.39 × 10−2 |
15 | 1.50 × 10−1 | 2.33 × 105 | 3.40 × 10−4 |
16 | 1.90 × 10−1 | 2.29 × 105 | 4.12 × 10−3 |
17 | 2.50 × 10−1 | 2.36 × 105 | 2.06 × 10−2 |
18 | 3.20 × 10−1 | 2.57 × 105 | 5.49 × 10−2 |
19 | 4.30 × 10−1 | 3.04 × 105 | 8.23 × 10−2 |
20 | 6.90 × 10−1 | 4.34 × 105 | 6.58 × 10−2 |
21 | 6.92 | 4.49 × 106 | 2.20 × 10−2 |
VP | Marine Coastal Farm | Hypermarket | Farm Water | ||||||
---|---|---|---|---|---|---|---|---|---|
Sample Total | Gill | Skin | Intestine | Sample Total | Gill | Skin | Intestine | ||
Occurrence—haemolytic | 45 | 8/15 (18) | 0/15 (0) | 5/15 (11) | 45 | 12/15 (27) | 4/15 (9) | 11/15 (24) | 2/6 (33) |
Mean Concentration —haemolytic | - | 3.3 (0.39) | 0 (0) | 3.6 (0.74) | - | 3.4 (0.38) | 2.3 (0.23) | 3.8 (0.24) | 3.0 (0.035) |
Occurrence—AMP-R | 45 | 1/15 (2) | 0/15 (0) | 0/15 (0) | 45 | 12/15 (27) | 4/15 (9) | 0/15 (0) | 2/6 (33) |
Mean Concentration—AMP-R | - | 2.3 (0) | 0 (0) | 0 (0) | - | 3.7 (0.33) | 2.3 (0.23) | 3.7 (0.32) | 2.7 (0.41) |
Occurrence—PENG-R | 45 | 2/15 (4) | 0/15 (0) | 0/15 (0) | 45 | 9/15 (20) | 7/15 (16) | 10/15 (22) | 2/6 (33) |
Mean Concentration—PENG-R | - | 2.2 (0.15) | 0 (0) | 0 (0) | - | 3.0 (0.21) | 1.9 (0.12) | 4.1 (0.43) | 2.0 (0) |
Occurrence—TET-R | 45 | 0/15 (0) | 0/15 (0) | 0/15 (0) | 45 | 12/15 (27) | 0/15 (0) | 9/15 (20) | 0/6 (0) |
Mean Concentration—TET-R | - | 0 (0) | 0 (0) | 0 (0) | - | 2.1 (0.20) | 0 (0) | 3.0 (0.49) | 0 (0) |
Farm-to-Home | Retail-to-Home | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
Haemolytic | Ampicillin | Penicillin G | Tetracycline | Haemolytic | Ampicillin | Penicillin G | Tetracycline | |||
Occurrence (Farm/Retail) | 2.9 × 10−1 (1.9 × 10−1, 4.1 × 10−1) | 4.3 × 10−2 (7.8 × 10−3, 9.9 × 10−2) | 6.4 × 10−2 (1.8 × 10−2, 1.3 × 10−1) | N.A. | 6.0 × 10−1 (4.8 × 10−1, 7.1 × 10−1) | 5.7 × 10−1 (4.6 × 10−1, 6.9 × 10−1) | 5.7 × 10−1 (4.6 × 10−1, 6.9 × 10−1) | 4.7 × 10−1 (3.5 × 10−1, 5.9 × 10−1) | ||
Concentra-tion (LogCFU/g) | Farm | Pre-harvest | 2.4 (6.5 × 10−1, 4.5) | 6.8 × 10−1 (0, 1.9) | 4.5 × 10−1 (0, 8.6 × 10−1) | N.A. | N.A. | N.A. | N.A. | N.A. |
Post-harvest | 2.9 (1.1, 4.9) | 1.2 (3.7 × 10−1, 2.4) | 9.2 × 10−1 (4.6 × 10−1, 1.4) | N.A. | N.A. | N.A. | N.A. | N.A. | ||
Retail | Retail-start | 2.9 (1.1, 5.0) | 1.2 (3.8 × 10−1, 2.4) | 9.3 × 10−1 (4.7 × 10−1, 1.4) | N.A. | 2.7 (1.5, 4.1) | 2.8 (1.6, 4.2) | 2.7 (1.3, 4.5) | 1.6 (1.0 × 10−1, 3.6) | |
Retail-end | 3.0 (1.2, 5.0) | 1.2 (4.1 × 10−1, 2.4) | 9.7 × 10−1 (5.1 × 10−1, 1.4) | N.A. | 2.7 (1.6, 4.1) | 2.8 (1.6, 4.3) | 2.7 (1.4, 4.6) | 1.7 (1.4 × 10−1, 3.7) | ||
Home | Home | 3.1 (1.3, 5.1) | 1.35 (5.6 × 10−1, 2.6) | 1.1 (6.6 × 10−1, 1.6) | N.A. | 2.9 (1.7, 4.3) | 3.0 (1.8, 4.4) | 2.8 (1.5, 4.7) | 1.8 (3.0 × 10−1, 3.8) | |
Preparation | Average Washing | 1.3 (0, 3.5) | 1.6 × 10−1 (0, 1.0) | 4.9 × 10−2 (0, 4.0 × 10−1) | N.A. | 1.0 (0, 2.7) | 1.2 (0, 2.9) | 1.1 (0, 3.0) | 4.5 × 10−1 (0, 2.1) | |
Washing | 1.2 (0, 3.3) | 1.1 × 10−1 (0, 7.8 × 10−1) | 1.2 × 10−2 (0, 1.5 × 10−2) | N.A. | 9.2 × 10−1 (0, 2.4) | 1.1 (0, 2.6) | 9.5 × 10−1 (0, 2.9) | 3.8 × 10−1 (0, 2.0) | ||
No washing | 2.3 (2.9 × 10−1, 4.4) | 6.2 × 10−1 (0, 1.9) | 3.8 × 10−1 (0, 1.2) | N.A. | 2.0 (5.9 × 10−1, 3.6) | 2.1 (6.6 × 10−1, 3.8) | 2.0 (4.0 × 10−1, 4.0) | 1.1 (0, 3.1) | ||
Cooking | Average Washing | 8.9 × 10−2 (0, 6.8 × 10−1) | 1.3 × 10−3 (0, 0) | 3.4 × 10−5 (0, 0) | N.A. | 3.7 × 10−2 (0, 7.6 × 10−2) | 4.7 × 10−2 (0, 2.5 × 10−1) | 5.5 × 10−2 (0, 2.7 × 10−1) | 1.7 × 10−2 (0, 0) | |
Washing | 7.3 × 10−2 (0, 5.1 × 10−1) | 4.5 × 10−4 (0, 0) | 2.5 × 10−7 (0, 0) | N.A. | 2.6 × 10−2 (0, 0) | 3.4 × 10−2 (0, 7.6 × 10−2) | 4.3 × 10−2 (0, 9.8 × 10−2) | 1.2 × 10−2 (0, 0) | ||
No washing | 2.4 × 10−1 (0, 1.7) | 9.3 × 10−3 (0, 0) | 3.7 × 10−4 (0, 0) | N.A. | 1.4 × 10−1 (0, 1.0) | 1.6 × 10−1 (0, 1.2) | 1.6 × 10−1 (0, 1.3) | 5.7 × 10−2 (0, 2.9 × 10−1) |
Farm-to-Home | Retail-to-Home | ||||||
---|---|---|---|---|---|---|---|
Pill,serving | Pill,yearly | Ncases | Pill,serving | Pill,yearly | Ncases | ||
Haemolytic | Average Washing | 2.9 × 10−4 (0, 9.0 × 10−5) | 1.6 × 10−2 (0, 3.5 × 10−2) | 1.5 × 102 (0, 3.2 × 102) | 4.5 × 10−5 (0, 8.4 × 10−6) | 6.3 × 10−3 (0, 3.6 × 10−4) | 5.7 × 101 (0, 3.3) |
Washing | 1.9 × 10−4 (0, 5.7 × 10−5) | 1.3 × 10−2 (0, 2.1 × 10−2) | 1.2 × 102 (0, 1.9 × 102) | 2.4 × 10−5 (0, 0) | 4.3 × 10−3 (0, 0) | 3.8 × 101 (0, 0) | |
No washing | 1.1 × 10−3 (0, 8.6 × 10−4) | 4.7 × 10−2 (0, 3.2 × 10−1) | 4.2 × 102 (0, 2.8 × 103) | 2.5 × 10−4 (0, 2.6 × 10−4) | 2.5 × 10−2 (0, 1.1 × 10−1) | 2.3 × 102 (0, 1.0 × 103) | |
Haemolytic and AMP-R | Average Washing | 4.5 × 10−7 (0, 0) | 1.8 × 10−4 (0, 0) | 1.6 (0, 0) | 5.2 × 10−5 (0, 2.7 × 10−5) | 8.0 × 10−3 (0, 7.9 × 10−3) | 7.2 × 101 (0, 7.1 × 101) |
Washing | 1.3 × 10−7 (0, 0) | 5.9 × 10−5 (0, 0) | 5.3 × 10−1 (0, 0) | 2.6 × 10−5 (0, 8.3 × 10−6) | 5.4 × 10−3 (0, 4.9 × 10−4) | 4.9 × 101 (0, 4.4) | |
No washing | 3.4 × 10−6 (0, 0) | 1.3 × 10−3 (0, 0) | 1.1 × 101 (0, 0) | 2.8 × 10−4 (0, 3.7 × 10−4) | 3.1 × 10−2 (0, 1.6 × 10−1) | 2.8 × 102 (0, 1.4 × 103) | |
Haemolytic and PENG-R | Average Washing | 1.0 × 10−8 (0, 0) | 5.6 × 10−6 (0, 0) | 5.0 × 10−2 (0, 0) | 1.2 × 10−4 (0, 2.8 × 10−5) | 1.0 × 10−2 (0, 7.7 × 10−3) | 9.1 × 101 (0, 7.0 × 101) |
Washing | 7.2 × 10−11 (0, 0) | 5.3 × 10−8 (0, 0) | 4.8 × 10−4 (0, 0) | 7.4 × 10−5 (0, 9.8 × 10−6) | 7.7 × 10−3 (0, 6.7 × 10−4) | 6.9 × 101 (0, 6.1) | |
No washing | 1.0 × 10−7 (0, 0) | 5.4 × 10−5 (0, 0) | 4.9 × 10−1 (0, 0) | 5.7 × 10−4 (0, 3.8 × 10−4) | 3.2 × 10−2 (0, 1.5 × 10−1) | 2.9 × 102 (0, 1.4 × 103) | |
Haemolytic and TET-R | Average Washing | N.A. | N.A. | N.A. | 2.3 × 10−5 (0, 0) | 2.6 × 10−3 (0, 0) | 2.4 × 101 (0, 0) |
Washing | N.A. | N.A. | N.A. | 1.3 × 10−5 (0, 0) | 1.9 × 10−3 (0, 0) | 1.7 × 101 (0, 0) | |
No washing | N.A. | N.A. | N.A. | 1.1 × 10−4 (0, 2.5 × 10−5) | 9.4 × 10−3 (0, 7.0 × 10−3) | 8.5 × 101 (0, 6.3 × 101) |
Farm-to-Home | Retail-to-Home | ||
---|---|---|---|
Haemolytic | Average washing | 1 | 1 |
Washing | 1 | 1 | |
No washing | 1 | 1 | |
Ampicillin | Average washing | 1.1 × 10−2 | 1.3 |
Washing | 4.5 × 10−3 | 1.3 | |
No washing | 2.7 × 10−2 | 1.2 | |
Penicillin G | Average washing | 3.4 × 10−4 | 1.6 |
Washing | 4.1 × 10−6 | 1.8 | |
No washing | 1.2 × 10−3 | 1.3 | |
Tetracycline | Average washing | NA | 4.2 × 10−1 |
Washing | NA | 4.4 × 10−1 | |
No washing | NA | 3.8 × 10−1 |
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Ong, H.M.G.; Zhong, Y.; Hu, C.C.; Ong, K.H.; Khor, W.C.; Schlundt, J.; Aung, K.T. Quantitative Risk Evaluation of Antimicrobial-Resistant Vibrio parahaemolyticus Isolated from Farmed Grey Mullets in Singapore. Pathogens 2023, 12, 93. https://doi.org/10.3390/pathogens12010093
Ong HMG, Zhong Y, Hu CC, Ong KH, Khor WC, Schlundt J, Aung KT. Quantitative Risk Evaluation of Antimicrobial-Resistant Vibrio parahaemolyticus Isolated from Farmed Grey Mullets in Singapore. Pathogens. 2023; 12(1):93. https://doi.org/10.3390/pathogens12010093
Chicago/Turabian StyleOng, Hong Ming Glendon, Yang Zhong, Cheng Cheng Hu, Kar Hui Ong, Wei Ching Khor, Joergen Schlundt, and Kyaw Thu Aung. 2023. "Quantitative Risk Evaluation of Antimicrobial-Resistant Vibrio parahaemolyticus Isolated from Farmed Grey Mullets in Singapore" Pathogens 12, no. 1: 93. https://doi.org/10.3390/pathogens12010093
APA StyleOng, H. M. G., Zhong, Y., Hu, C. C., Ong, K. H., Khor, W. C., Schlundt, J., & Aung, K. T. (2023). Quantitative Risk Evaluation of Antimicrobial-Resistant Vibrio parahaemolyticus Isolated from Farmed Grey Mullets in Singapore. Pathogens, 12(1), 93. https://doi.org/10.3390/pathogens12010093