One Health Determinants of Escherichia coli Antimicrobial Resistance in Humans in the Community: An Umbrella Review
Abstract
:1. Introduction
2. Results
2.1. Review Characteristics
2.2. Quality Assessment
2.3. Human Variables
2.3.1. Antibiotic Use
2.3.2. Comorbidities, Medication Use, and Hospitalization
2.3.3. Diet, Sex, Age, and Living
2.3.4. Travel
2.4. Animal and Environmental Variables
2.5. Temporal Relationship Variable and AMR E. coli
3. Discussion
4. Materials and Methods
4.1. The Search Strategy and Selection Criteria
4.2. Data Extraction
4.3. Assessment of Methodological Quality
4.4. Data Synthesis
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Study ID | Total Number of Studies That Fulfilled Inclusion Criteria in Umbrella Review (Total Number of Studies in Review) | One Health Category | Population | Continent(s) |
---|---|---|---|---|
Alividza 2018 [34] | 11 (19) | Human | Any age group | Asia, Europe, South America |
Bakhit 2018 [35] | 3 (25) | Human | Any age group | Europe, South America |
Bell 2014 [36] | 243 (243) | Human | Any age group | Europe, North America, Other 1 |
Bhate 2021 [37] | 2 (5) | Human | Aged ≥ 8 years with acne | Europe |
Bryce 2016 [38] | 6 (34) | Human | Children and adolescents (0–17 years old) | Asia, North America, South America |
Bryce 2016 [39] | 5 (58) | Human | Children and adolescents (0–17 years old) | Asia, Europe, North America |
Butcher 2019 [40] | 15 (34) | Human | Any age group | Asia, Europe, South America |
Chan 2022 [41] | 25 (25) | Human | Children and adolescents (0–18 years old) | Asia |
Costelloe 2010 [42] | 8 (24) | Human | Any age group | NR |
Furuya-Kanamori 2020 [43] | 20 (20) | Human | International travelers | Asia, Europe, North America, Oceania |
Hackmann 2021 [44] | 23 (23) | Animal | Any pet | Asia, Europe, North America, South America |
Hassing 2015 [45] | 11 (11) | Human | Asymptomatic travelers | Europe, North America, Oceania |
Hu 2020 [15] | 15 (15) | Human | Healthy population aged 18–65 | Africa, Asia, Europe |
Karanika 2016 [46] | 66 (66) | Human | Healthy individuals | Africa, Asia, Europe, North America, South America, Oceania |
Köck 2018 [47] | 2 (68) | Animal | Wildlife, food-producing, and companion animals | Asia, Africa |
Larramendy 2020 [48] | 16 (16) | Human and Environment | Any age group | Africa, Asia, Europe, South America |
Lazarus 2015 [49] | 34 (34) | Animal | Food-producing animals | Global 2 |
Messina 2020 [50] | 4 (30) | Human | Healthy children and adolescents (0–21 years old) | Asia, Europe, North America, Oceania |
O’Brien 2019 [51] | 3 (19) | Human | Children (1 month to 5 years old) | Africa |
Ramblière 2021 [52] | 3 (36) | Human | Children (0–15 months old) exposed to HIV and HIV-infected adults | Africa |
Truong 2022 [53] | 2 (7) | Human | Oral daily tetracycline users | Africa, Asia |
Voor In ‘t Holt 2020 [54] | 22 (22) | Human | Travelers without infection | Asia, Europe, North America, Oceania |
Willems 2020 [55] | 4 (26) | Human | Acid suppressant users | Europe |
Variable | Subcategory | Number of Participants (Number of Studies Investigating Variable) | Magnitude of Association OR (95% CI) | Importance Rating * |
---|---|---|---|---|
Antibiotic use | General antibiotic use | 6 studies (NR) | 1.51 (1.17–1.94) [15] | + |
1528 (6 studies) | 1.58 ** (1.16–2.16) [46] | |||
1297 (5 studies) | 1.63 ** (1.19–2.24) [46] | |||
449 (1 study) | 1.8 (1.0–3.1) [48] | |||
88 studies (NR) | 2.33 (2.19–2.49) [36] | |||
NR (5 studies) | 2.65 (1.70–4.12) [41] | |||
172 (1 study) | 3.1 (1.4–6.7) [48] | |||
484 (1 study) | 4.0 (1.6–10.0) [48] | |||
300 (1 study) | 4.6 (1.9–11.0) [48] | |||
140 (1 study) | 5.6 (2.1–14.8) [48] | |||
Trimethoprim and β-lactams | 179 (2 studies) | 3.2 (0.9–10.8) [35] | 0 | |
Beta-Lactam | 290 (1 study) | 4.5 (1.8–11.0) [48] | +++ | |
510 (1 study) | 4.6 (2.0–10.7) [48] | |||
(Fluoro)Quinolone | 449 (1 study) | 2.1 (0.6–7.3) [48] | + | |
200 (1 study) | 2.6 (1.3–5.1) [48] | |||
140 (1 study) | 9.9 (2.2–44.6) [48] | |||
290 (1 study) | 19.0 (3.3–111.4) [48] | |||
Penicillin | 7170 (1 study) | 0.9 (0.5–1.7) [48] | 0 | |
408 (1 study) | 2.7 (1.2–6.3) [48] | |||
Cephalosporin | 74 (1 study) | 1.5 (5.4–85.2) [48] | + | |
200 (1 study) | 2.2 (1.01–5.0) [48] | |||
408 (1 study) | 2.2 (1.1–4.5) [48] | |||
200 (1 study) | 3.9 (1.8–8.5) [48] | |||
Macrolides | 7170 (1 study) | 1.5 (1.1–2.2) [48] | 0 | |
Nitrofurantoin | 7170 (1 study) | 1.54 (1.1–2.3) [48] | 0 | |
Longer duration of course (>7 days vs. <7 days amoxicillin and trimethoprim) | 1521 (2 studies) | 1.50 (0.76–2.92) [42] | 0 | |
1521 (2 studies) | 2.89 (1.44–5.78) [42] | |||
Multiple courses (>3 courses vs. 1 course, trimethoprim, amoxicillin, trimethoprim) | 1521 (2 studies) | 0.4 (0.12–1.31) [42] | ++ | |
1521 (2 studies) | 3.95 (1.06–14.72) [42] | |||
1521 (2 studies) | 3.62 (1.25–10.48) [42] | |||
Mass administration | NR (1 study) | 3.64 (2.38–5.78) [51] | +++ | |
NR (5 studies) | 7.8 (3.0–20.2) [52] | |||
NR (5 studies) | 10.2 (5.9–17.8) [52] | |||
NR (5 studies) | 17.1 (2.3–127.7) [52] | |||
Higher dose (each 200 mg trimethoprim tablet extra and 500 mg instead of 250 mg amoxicillin) | 1521 (2 studies) | 1.01 (1.01–1.02) [42] | + | |
1521 (2 studies) | 2.26 (1.13–4.55) [42] | |||
Comorbidities | Previous/recurrent UTI | 7170 (1 study) | 1.3 (1.01–1.6) [48] | ++ |
408 (1 study) | 3.4 (1.8–6.7) [48] | |||
510 (1 study) | 3.8 (1.8–8.1) [48] | |||
Previous/recurrent pyelonephritis | 300 (1 study) | 1.7 (0.7–3.9) [48] | − | |
Previous catheterization | 408 (1 study) | 3.3 (1.7–6.6) [48] | + | |
Diarrhea symptoms | 5144 (7 studies) | 1.53 (1.27–1.84) [15] | 0 | |
Diabetes | 300 (1 study) | 1.7 (0.8–3.4) [48] | ++ | |
290 (1 study) | 3.7 (1.1–12.7) [48] | |||
484 (1 study) | 3.0 (1.1–8.0) [48] | |||
Recurrent acute pyelonephritis and a history of diabetes | 300 (1 study) | 4.2 (1.3–16.9) [48] | + | |
Renal or urological disorder | 7170 (1 study) | 1.6 (1.0–2.5) [48] | − | |
484 (1 study) | 3.5 (1.0–11.5) [48] | |||
History prostatic disease | 510 (1 study) | 9.6 (2.1–44.8) [48] | + | |
Chronic disease | 2323 (3 studies) | 0.91 (0.13–6.53) [15] | − | |
Medication use | Immunosuppressive therapy | 7170 (1 study) | 1.5 (1.1–2.1) [48] | 0 |
Corticosteroids | 172 (1 study) | 24.3 (2.4–246.9) [48] | + | |
Acid suppressants | 4111 (3 studies) | 1.31 (0.11–15.5) [15] | 0 | |
NR (4 studies) | 1.41 (1.07–1.87) [55] | |||
Hospitalization | Previous hospitalization | 1379 (5 studies) | 1.18 ** (0.78–1.81) [46] | + |
1163 (4 studies) | 1.28 ** (0.82–2.03) [46] | |||
7170 (1 study) | 1.7 (1.3–2.3) [48] | |||
172 (1 study) | 2.9 (1.3–6.6) [48] | |||
7170 (1 study) | 3.9 (2.6–5.8) [48] | |||
449 (1 study) | 3.9 (1.2–12.7) [48] | |||
Prior surgery | 172 (1 study) | 2.8 (1.9–8.0) [48] | 0 | |
Diet | Vegetarian | 6802 (5 studies) | 1.60 (1.0043–2.5587) [15] | 0 |
Raw milk | 226 (1 study) | 7.54 (2.41–23.45) [15] | + | |
Fish | 290 (1 study) | 0.6 (0.5–0.9) [48] | 0 | |
Sex and age | Older age | 300 (1 study) | 2.0 (1.02–3.5) [48] | 0 |
Male sex | NR (9 studies) | 0.96 (0.74–1.24) [41] | 0 | |
7170 (1 study) | 1.6 (1.2–2.1) [48] |
Variable | Subcategory | Number of Participants (Number of Studies Investigating Variable) | Magnitude of Association OR (95% CI) | Importance Rating * |
---|---|---|---|---|
Living standards | Lower socioeconomic status | 2775 (1 study) | 1.33 (1.07–1.75) [34] | + |
2775 (1 study) | 2.47 (1.08–5.66) [34] | |||
Day-care attendance | NR (6 studies) | 1.49 (1.17–1.91) [41] | 0 | |
Living in Northern vs. Southern Europe | 7170 (1 study) | 0.4 (0.2–0.7) [48] | 0 | |
Travel | International travel | 1887 (6 studies) | 4.06 ** (1.33–2.41) [46] | +++ |
834 (1 study) | 21 (4.5–97) [48] | |||
To Asia | NR (4 studies) | 1.78 (0.64–4.98) [15] | ++ | |
NR (12 studies) | 14.16 (5.50–36.45) [54] | |||
370 (1 study) | 30.0 (6.3–147.2) [45] | |||
To Africa | NR (3 studies) | 0.94 ** (0.14–6.17) [46] | − | |
To India | 182 (3 studies) | 2.4 ** (1.26–4.58) [46] | + | |
NR (3 studies) | 3.80 (2.23–6.47) [15] | |||
Health while traveling | Inflammatory bowel disease | 5253 (20 studies) | 2.09 (1.16–3.77) [43] | 0 |
Diarrhea | NR (4 studies) | 1.65 (1.02–2.68) [15] | + | |
5253 (20 studies) | 1.69 (1.25–2.30) [43] | |||
NR (12 studies) | 2.02 (1.45–2.81) [54] | |||
430 (1 study) | 31.0 (2.7–358.1) [45] | |||
Contact with healthcare while traveling | 5253 (20 studies) | 1.53 (1.09–2.15) [43] | 0 | |
Antibiotic use | 5253 (20 studies) | 2.38 (1.88–3.00) [43] | + | |
NR (12 studies) | 2.78 (1.76–4.39) [54] | |||
NR (4 studies) | 2.81 (1.47–5.36) [15] | |||
99 (1 study) | 3.0 (1.4–6.7) [45] | |||
99 (1 study) | 5.0 (1.1–26.2) [45] | |||
Traveler demographics | Backpackers compared to other travelers | 5253 (20 studies) | 1.46 (1.20–1.78) [43] | 0 |
Vegetarian diet | 5253 (20 studies) | 1.41 (1.01–1.96) [43] | + | |
NR (3 studies) | 1.92 (1.13–3.26) [15] | |||
Diet associated with risk (pastry, meals from stalls, etc.) | NR (12 studies) | 1.27 (0.67–2.41) [54] | − | |
Street food consumption | NR (2 studies) | 0.92 (0.49–1.74) [15] | + | |
NR (2 studies) | 1.37 (1.08–1.73) [15] | |||
NR (2 studies) | 2.09 (1.30–3.38) [15] | |||
Raw vegetable consumption | NR (2 studies) | 0.34 (0.12–0.93) [15] | − | |
NR (2 studies) | 0.58 (0.33–1.07) [15] | |||
NR (2 studies) | 2.18 (1.29–3.68) [15] | |||
Protective measures while traveling | Consuming bottled water | 5253 (20 studies) | 1.29 (0.50–3.34) [43] | − |
General protective measures (disposable gloves, bottled water, etc.) | NR (12 studies) | 0.83 (0.61–1.13) [54] | − | |
Meticulous hand hygiene | 5253 (20 studies) | 1.10 (0.81–1.49) [43] | − | |
Probiotics | 5253 (20 studies) | 1.06 (0.78–1.45) [43] | − |
Animal | Subcategory | Number of Studies Investigating Variable (Number of Participants) | Magnitude of Association OR (95% CI) | Importance of Rating * |
---|---|---|---|---|
Pets | Pet owner | 963 (5 studies) | 1.39 ** (0.89–2.18) [44,46] | − |
9403 (12 studies) | 1.18 ** (0.83–1.68) [44] | |||
5159 (4 studies) | 1.15 (0.33–4.06) [15] | |||
Dog owner | 9403 (12 studies) | 0.88 ** (0.56–1.40) [44] | − | |
Cat owner | 9403 (12 studies) | 1.16 ** (0.58–2.34) [44] | − | |
Rodent owner | 9403 (12 studies) | 1.34 ** (0.43–4.18) [44] | − | |
Bird owner | 9403 (12 studies) | 0.91 ** (0.38–2.18) [44] | − | |
Environment | ||||
Freshwater | Swimming | 290 (1 study) | 2.1 (1.02–4.3) [48] | 0 |
Variable | Subcategory | Number of Studies Investigating Variable (Number of Participants) | Magnitude of Association OR (95% CI) | Importance of Rating * |
---|---|---|---|---|
Time after antibiotic use | One week | 129 (2 studies) | 7.1 (4.2–12) [35] | 0 |
Two weeks | NR (6 studies) | 1.08 (0.6–1.96) [38] | + | |
NR (1 study) | 6.12 (3.18–11.76) [39] | |||
One month | NR (6 studies) | 1.38 (1.16–1.64) [38] | ++ | |
93 (1 study) | 1.8 (0.9–3.6) [35] | |||
NR (1 study) | 6.20 (2.14–15.96) [39] | |||
NR (2 studies) | 8.38 (2.84–24.77) [39] | |||
1208 (3 studies) | 11.21 (7.13–17.63) [51] | |||
Two months | 14,348 (5 studies) | 2.5 (2.1–2.9) [42] | + | |
NR (1 study) | 5.08 (2.70–9.56) [38] | |||
Three months | NR (6 studies) | 1.65 (1.36–2.0) [38] | ++ | |
NR (1 study) | 3.38 (2.05–5.55) [39] | |||
1208 (3 studies) | 10.64 (3.79–29.92) [51] | |||
Six months | NR (1 study) | 3.16 (1.65–6.06) [39] | +++ | |
1208 (3 studies) | 4.76 (1.52–14.90) [51] | |||
NR (1 study) | 13.23 (7.84–22.31) [39] | |||
12 months 11, 51, 54, 59, 60 | 14,348 (5 studies) | 1.33 (1.2–1.5) [42] | + | |
NR (1 study) | 0.94 (0.57–1.56) [39] | |||
10,079 (13 studies) | 1.84 (1.35–2.51) [15] | |||
NR (1 study) | 1.89 (1.04–3.42) [39] | |||
Over 12 months | NR (1 study) | 0.94 (0.57–1.56) [39] | − | |
Time after return from travel | Six weeks | 290 (1 study) | 16.4 (3.4–78.8) [48] | + |
Between six weeks and two years | 290 (1 study) | 2.2 (1.1–4.3) [48] | 0 |
Category of Importance of Variable | Grading Criteria * |
---|---|
Very strong association: +++ | The variable is associated with AMR E. coli in all reviews, without exception. More than one study included in the review(s) needed to show a significant association and a moderate effect size of OR/RR ** ≥ 3.0. |
Strong association: ++ | One study, or more than 50% of the studies included in the review(s), showed a significant association between the variable and AMR E. coli with a moderate effect size of OR/RR ≥ 3.0. |
Moderate association: + | The variable is associated with AMR E. coli in a single study or in ≤ 50% of studies in the review(s) with a significant moderate effect size of OR/RR ≥ 3.0. Or the variable is associated with AMR E. coli in >50% of the studies with a small significant effect size of OR/RR < 3.0. |
Weak association: 0 | The variable is associated with AMR E. coli in a single study or in ≤50% of studies in the review(s) with a moderate significant effect size of OR/RR < 3.0. Or the variable is associated with AMR E. coli in >50% of the studies with a moderate nonsignificant effect size of OR/RR ≥ 3.0. |
No association: − | One study, or more than 50% of the studies included in the review(s), showed an association between the variable and AMR E. coli with a small nonsignificant effect size of OR/RR < 3.0. |
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Share and Cite
Smit, C.C.H.; Lambert, M.; Rogers, K.; Djordjevic, S.P.; Van Oijen, A.M.; Keighley, C.; Taxis, K.; Robertson, H.; Pont, L.G. One Health Determinants of Escherichia coli Antimicrobial Resistance in Humans in the Community: An Umbrella Review. Int. J. Mol. Sci. 2023, 24, 17204. https://doi.org/10.3390/ijms242417204
Smit CCH, Lambert M, Rogers K, Djordjevic SP, Van Oijen AM, Keighley C, Taxis K, Robertson H, Pont LG. One Health Determinants of Escherichia coli Antimicrobial Resistance in Humans in the Community: An Umbrella Review. International Journal of Molecular Sciences. 2023; 24(24):17204. https://doi.org/10.3390/ijms242417204
Chicago/Turabian StyleSmit, Chloé C. H., Maarten Lambert, Kris Rogers, Steven P. Djordjevic, Antoine M. Van Oijen, Caitlin Keighley, Katja Taxis, Hamish Robertson, and Lisa G. Pont. 2023. "One Health Determinants of Escherichia coli Antimicrobial Resistance in Humans in the Community: An Umbrella Review" International Journal of Molecular Sciences 24, no. 24: 17204. https://doi.org/10.3390/ijms242417204