A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance

Bell, Brian G; Schellevis, Francois; Stobberingh, Ellen; Goossens, Herman; Pringle, Mike

doi:10.1186/1471-2334-14-13

Cited by 1,262Antibiotic Use and ResistanceAntibiotic Resistance in BacteriaPharmaceutical and Antibiotic Environmental Impacts

A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance

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Bell, Brian G, Schellevis, Francois, Stobberingh, Ellen, Goossens, Herman, Pringle, Mike·2014·BMC Infectious Diseases

DOI 10.1186/1471-2334-14-13PMC PMC3897982

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Abstract

BACKGROUND: Greater use of antibiotics during the past 50 years has exerted selective pressure on susceptible bacteria and may have favoured the survival of resistant strains. Existing information on antibiotic resistance patterns from pathogens circulating among community-based patients is substantially less than from hospitalized patients on whom guidelines are often based. We therefore chose to assess the relationship between the antibiotic resistance pattern of bacteria circulating in the community and the consumption of antibiotics in the community. METHODS: Both gray literature and published scientific literature in English and other European languages was examined. Multiple regression analysis was used to analyse whether studies found a positive relationship between antibiotic consumption and resistance. A subsequent meta-analysis and meta-regression was conducted for studies for which a common effect size measure (odds ratio) could be calculated. RESULTS: Electronic searches identified 974 studies but only 243 studies were considered eligible for inclusion by the two independent reviewers who extracted the data. A binomial test revealed a positive relationship between antibiotic consumption and resistance (p < .001) but multiple regression modelling did not produce any significant predictors of study outcome. The meta-analysis generated a significant pooled odds ratio of 2.3 (95% confidence interval 2.2 to 2.5) with a meta-regression producing several significant predictors (F(10,77) = 5.82, p < .01). Countries in southern Europe produced a stronger link between consumption and resistance than other regions. CONCLUSIONS: Using a large set of studies we found that antibiotic consumption is associated with the development of antibiotic resistance. A subsequent meta-analysis, with a subsample of the studies, generated several significant predictors. Countries in southern Europe produced a stronger link between consumption and resistance than other regions so efforts at reducing antibiotic consumption may need to be strengthened in this area. Increased consumption of antibiotics may not only produce greater resistance at the individual patient level but may also produce greater resistance at the community, country, and regional levels, which can harm individual patients.

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Fast de-escalation was shown to be associated with a decreased risk.
“and a fast de-escalation was shown to be associated with a decreased risk [26, 27].”
From Lab efficiency and improvements in the management of bloodstream infections: a before and after study (2025) · cites this paper as [26]
The Discussion (page unavailable) reports that decreased antibiotic consumption was associated with decreased bacterial resistance. It does not establish that fast de-escalation specifically was associated with decreased risk; a search for de-escalation found no such finding in our copy. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Antibiotic resistance is correlated with antibiotic use.
“Antibiotic resistance being correlated with antibiotic use, in terms of antimicrobial stewardship, it is crucial that antibiotics are only used when indicated”
From Lab efficiency and improvements in the management of bloodstream infections: a before and after study (2025) · cites this paper as [26]

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Jakobsson, H. E., Wreiber, K., Fall, K., Fjelstad, B., Nyrén, O., & Engstrand, L. G. (2007) · Scandinavian Journal of Infectious Diseases · doi:10.1080/00365540701299608 · Cited by 40 · see citing works
Risk Factors for Development of Multiple-Class Resistance to Streptococcus pneumoniae Strains in Belgium over a 10-Year Period: Antimicrobial Consumption, Population Density, and Geographic Location
Eldere, J. V., Mera, R. M., Miller, L. A., Poupard, J. A., & Amrine‐Madsen, H. (2007) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01581-06 · Cited by 40 · see citing works
Factors Associated With Antimicrobial Resistance and Mortality in Pneumococcal Bacteremia
Neuman, M. I., Kelley, M., Harper, M. B., File, T. M., & Camargo, C. A. (2007) · Journal of Emergency Medicine · doi:10.1016/j.jemermed.2006.08.014 · Cited by 40 · see citing works
The Association Between Antibiotic Use in the Community and Nasopharyngeal Carriage of Antibiotic-Resistant Streptococcus pneumoniae in Bedouin Children
Greenberg, D., Givon‐Lavi, N., Sharf, A., Vardy, D., & Dagan, R. (2008) · The Pediatric Infectious Disease Journal · doi:10.1097/inf.0b013e3181715184 · Cited by 37 · see citing works
Antimicrobial Use and Serotype Distribution of NasopharyngealStreptococcus pneumoniaeIsolates Recovered from Greek Children Younger than 2 Years Old
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Risk Factors for the Nasopharyngeal Carriage of Respiratory Pathogens by Portuguese Children: Phenotype and Antimicrobial Susceptibility of Haemophilus influenzae and Streptococcus pneumoniae
Neto, A. S., Lavado, P., Flores, P., Dias, R. P. M., Pessanha, M. A., Sousa, E. N., Palminha, J. M., Caniça, M., & Pina, J. E. (2003) · Microbial Drug Resistance · doi:10.1089/107662903764736409 · Cited by 37 · see citing works
Risk factors for nasopharyngeal carriage of drug-resistant Streptococcus pneumoniae: data from a nation-wide surveillance study in Greece
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Quinolone resistance among Escherichia coli strains from community-acquired urinary tract infections in Greece
Chaniotaki, S., Giakouppi, P., TZOUVELEKIS, L. S., Panagiotakos, D. B., Kozanitou, M., Petrikkos, G. L., Avlami, A., & Vatopoulos, A. C. (2004) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2004.00807.x · Cited by 36 · see citing works
Household contacts were key factor for children's colonization with resistant Escherichia coli in community setting
Lietzau, S., Raum, E., von Baum, H., Marre, R., & Brenner, H. (2007) · Journal of Clinical Epidemiology · doi:10.1016/j.jclinepi.2007.01.016 · Cited by 35 · see citing works
Decreased Erythromycin Use after Antimicrobial Reimbursement Restriction for Undocumented Bacterial Upper Respiratory Tract Infections Significantly Reduced Erythromycin Resistance in Streptococcus pyogenes in Taiwan
Hsueh, P., Shyr, J.-M., & Wu, J.-J. (2005) · Clinical Infectious Diseases · doi:10.1086/427946 · Cited by 35 · see citing works
Connection between Trimethoprim-Sulfamethoxazole Use and Resistance in Streptococcus pneumoniae, Haemophilus influenzae , and Moraxella catarrhalis
Kärpänoja, P., Nyberg, S. T., Bergman, M., Voipio, T., Paakkari, P., Huovinen, P., & Sarkkinen, H. (2008) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01118-07 · Cited by 35 · see citing works
Risk factors for urinary tract infections due to ciprofloxacin-resistant Escherichia coli in a tertiary care urology department in Switzerland
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Changes in macrolide resistance among respiratory pathogens after decreased erythromycin consumption in Taiwan
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MONTHLY CHANGES IN THE RATE OF RECOVERY OF PENICILLIN-RESISTANT ORGANISMS FROM CHILDREN
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Methicillin-resistant Staphylococcus aureus: prevalence, incidence and risk factors associated with colonization in Sri Lanka
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Antibiotic use and resistance of Streptococcus pneumoniae in The Netherlands during the period 1994-1999
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Invasive Penicillin-Resistant Pneumococcal Infections:
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Macrolide Prescriptions and Erythromycin Resistance of Streptococcus pyogenes
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Beta-Lactamase Production in the Upper Respiratory Tract Flora in Relation to Antibiotic Consumption: A Study in Children Attending Day Nurseries
Mölstad, S., Eliasson, I., Hovelius, B., Kamme, C., & Schalén, C. (1988) · Scandinavian Journal of Infectious Diseases · doi:10.3109/00365548809032459 · Cited by 30 · see citing works
Utilization of fluoroquinolones andEscherichia coli resistance in urinary tract infection: inpatients and outpatients
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High‐Level Penicillin‐NonsusceptibleStreptococcus pneumoniaeBacteremia: Identification of a Low‐Risk Subgroup
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Relation between beta-lactamase producing bacteria and patient characteristics in chronic obstructive pulmonary disease (COPD).
Sportel, J. H., Koëter, G. H., van Altena, R., Löwenberg, A., & Boersma, W. (1995) · Thorax · doi:10.1136/thx.50.3.249 · Cited by 27 · see citing works
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Costelloe, C., Lovering, A. M., Montgomery, A. A., Lewis, D., McNulty, C. A. M., & Hay, A. D. (2011) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2011.09.022 · Cited by 26 · see citing works
Demographic characteristics of patients with community-acquired bacteriuria and susceptibility of urinary pathogens to antimicrobials in northern Israel.
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Socioeconomic factors and antibiotic use in relation to antimicrobial resistance in the Amazonian area of Peru
Kristiansson, C., Grape, M., Gotuzzo, E., Samalvides, F., Chauca, J., Larsson, M., Bartoloni, A., Pallecchi, L., Kronvall, G., & Petzold, M. (2009) · Scandinavian Journal of Infectious Diseases · doi:10.1080/00365540902783301 · Cited by 25 · see citing works
Drug-resistant Escherichia coli , Rural Idaho
Hannah, E. L., Angulo, F. J., Johnson, J. R., Haddadin, B., Williamson, J., & Samore, M. H. (2005) · Emerging infectious diseases · doi:10.3201/eid1110.050140 · Cited by 25 · see citing works
Trends in penicillin and macrolide resistance among pneumococci in the UK and the Republic of Ireland in relation to antibiotic sales to pharmacies and dispensing doctors
Livermore, D. M., Reynolds, R., Stephens, P. J., Duckworth, G. J., Felmingham, D., Johnson, A. P., Murchan, S., Murphy, O. M., Gungabissoon, U., Waight, P., et al. (2006) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2006.05.025 · Cited by 24 · see citing works
Widespread Emergence of Methicillin Resistance in Community-acquired Staphylococcus aureus Infections in Denver
Clancy, M., Graepler, A., Breese, P. E., Price, C. S., & Burman, W. J. (2005) · Southern Medical Journal · doi:10.1097/01.smj.0000184800.83171.f7 · Cited by 22 · see citing works
Antibacterial Use and Streptococcus pneumoniae Penicillin Resistance: A Temporal Relationship Model
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Epidemiological Studies of Penicillin Resistance in Danish Staphylococcus aureus Strains in the period 1977 – 1990
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Impact of Amoxicillin on Pneumococcal Colonization Compared With Other Therapies for Acute Otitis Media
Toltzis, P., Dul, M. J., O’Riordan, M. A., Toltzis, H., & Blumer, J. L. (2005) · The Pediatric Infectious Disease Journal · doi:10.1097/01.inf.0000148880.61449.82 · Cited by 21 · see citing works
Trends in resistance to penicillin and erythromycin of invasive pneumococci in Portugal
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Decreasing rates of resistance to penicillin, but not erythromycin, in Streptococcus pneumoniae after introduction of a policy to restrict antibiotic usage in Taiwan
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Emergence of ciprofloxacin resistance in Escherichia coli isolates from outpatient urine samples
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Streptococcus pneumoniae antibiotic resistance in Northern Territory children in day care
Skull, S., Shelby‐James, T., Morris, P., Perez, G., Yonovitz, A., Krause, V., Roberts, L., & Leach, A. J. (1999) · Journal of Paediatrics and Child Health · doi:10.1046/j.1440-1754.1999.355400.x · Cited by 20 · see citing works
Community antibiotic therapy, hospitalization and subsequent respiratory tract isolation of Haemophilus influenzae resistant to amoxycillin: a nested case-control study
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Clustering of antibiotic resistance of E. coli in couples: suggestion for a major role of conjugal transmission
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Epidemiological Studies on Drug Resistance in Streptococcus pneumoniae in Hungary: An Update for the 1990s
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Prevalence and Patterns of Resistance of Streptococcus pneumoniae Strains Isolated from Carriers Attending Day Care Centers in the Area of Athens
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Resistance in Respiratory Tract Pathogens and Antimicrobial Use in Icelandic and Lithuanian Children
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Understanding the mechanisms and drivers of antimicrobial resistance
Holmes, A. H., Moore, L. S. P., Sundsfjord, A., Steinbakk, M., Regmi, S., Karkey, A., Guerin, P. J., & Piddock, L. J. V. (2015) · The Lancet · doi:10.1016/s0140-6736(15)00473-0 · Cited by 2,673 · see citing works
Association of adverse events with antibiotic use in hospitalized patients.
Tamma, P. D., Avdic, E., Li, D. X., Dzintars, K., & Cosgrove, S. E. (2017) · JAMA Internal Medicine · doi:10.1001/jamainternmed.2017.1938 · Cited by 800 · see citing works
Current evidence on hospital antimicrobial stewardship objectives: a systematic review and meta-analysis
Schuts, E. C., Hulscher, M., Mouton, J. W., Verduin, C. M., Stuart, J. W. T. C., Overdiek, H. W. P. M., van der Linden, P. D., Natsch, S., Hertogh, C. M. P. M., Wolfs, T. F. W., et al. (2016) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(16)00065-7 · Cited by 772 · see citing works
Anthropological and socioeconomic factors contributing to global antimicrobial resistance: a univariate and multivariable analysis
Collignon, P., Beggs, J. J., Walsh, T. R., Gandra, S., & Laxminarayan, R. (2018) · The Lancet Planetary Health · doi:10.1016/s2542-5196(18)30186-4 · Cited by 750 · see citing works
Global trends in antibiotic consumption during 2016–2023 and future projections through 2030
Klein, E. Y., Impalli, I., Poleon, S., Denoël, P., Cipriano, M., Boeckel, T. P. V., Pecetta, S., Bloom, D. E., & Nandi, A. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2411919121 · Cited by 481 · see citing works
Metal Resistance and Its Association With Antibiotic Resistance
Pal, C., Asiani, K., Arya, S., Rensing, C., Stekel, D. J., Larsson, D. G. J., & Hobman, J. L. (2017) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/bs.ampbs.2017.02.001 · Cited by 444 · see citing works
Quantifying drivers of antibiotic resistance in humans: a systematic review
Chatterjee, A., Modarai, M., Naylor, N. R., Boyd, S. E., Atun, R. A., Barlow, J. G., Holmes, A. H., Johnson, A. P., & Robotham, J. V. (2018) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(18)30296-2 · Cited by 388 · see citing works
Evolutionary Rescue
Bell, G. (2017) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-110316-023011 · Cited by 358 · see citing works
Antibiotic-Resistant Salmonella in the Food Supply and the Potential Role of Antibiotic Alternatives for Control
Nair, D. V. T., Venkitanarayanan, K., & Johny, A. K. (2018) · Foods · doi:10.3390/foods7100167 · Cited by 348 · see citing works
Biomaterials and Nanotherapeutics for Enhancing Skin Wound Healing
Das, S., & Baker, A. B. (2016) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2016.00082 · Cited by 331 · see citing works
Antibiotic strategies in the era of multidrug resistance
Karam, G. H., Chastre, J. E., Wilcox, M. H., & Vincent, J. (2016) · Critical Care · doi:10.1186/s13054-016-1320-7 · Cited by 297 · see citing works
Inappropriate empirical antibiotic therapy for bloodstream infections based on discordant in-vitro susceptibilities: a retrospective cohort analysis of prevalence, predictors, and mortality risk in US hospitals
Kadri, S. S., Lai, Y. L., Warner, S., Strich, J. R., Babiker, A., Ricotta, E., Demirkale, C. Y., Dekker, J. P., Palmore, T. N., Rhee, C., et al. (2020) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(20)30477-1 · Cited by 284 · see citing works
An international cross-sectional survey of antimicrobial stewardship programmes in hospitals
Howard, P., Pulcini, C., Hara, G. L., West, R. M., Gould, I. M., Harbarth, S., & Nathwani, D. (2014) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dku497 · Cited by 277 · see citing works
Rationalizing antimicrobial therapy in the ICU: a narrative review
Timsit, J., Bassetti, M., Cremer, O. L., Daikos, G. L., Waele, J. J. D., Kalil, A. C., Kipnis, É., Kollef, M. H., Laupland, K. B., Paiva, J.-A., et al. (2019) · Intensive Care Medicine · doi:10.1007/s00134-019-05520-5 · Cited by 275 · see citing works
Effect of C-Reactive Protein–Guided Antibiotic Treatment Duration, 7-Day Treatment, or 14-Day Treatment on 30-Day Clinical Failure Rate in Patients With Uncomplicated Gram-Negative Bacteremia: A Randomized Clinical Trial
von Dach, E., Albrich, W. C., Brunel, A.-S., Prendki, V., Cuvelier, C., Flury, D., Gayet-Ageron, A., Huttner, B., Kohler, P., Lemmenmeier, E., et al. (2020) · JAMA · doi:10.1001/jama.2020.6348 · Cited by 259 · see citing works
Current Knowledge on the Oxidative-Stress-Mediated Antimicrobial Properties of Metal-Based Nanoparticles
Mammari, N., Lamouroux, E., Boudier, A., & Duval, R. E. (2022) · Microorganisms · doi:10.3390/microorganisms10020437 · Cited by 255 · see citing works
Antimicrobial Resistance
Septimus, E. J. (2018) · Medical Clinics of North America · doi:10.1016/j.mcna.2018.04.005 · Cited by 247 · see citing works
Antibiotic resistance
MacGowan, A. P., & MacNaughton, E. (2017) · Medicine · doi:10.1016/j.mpmed.2017.07.006 · Cited by 246 · see citing works
Global antimicrobial-resistance drivers: an ecological country-level study at the human–animal interface
Allel, K., Day, L., Hamilton, A., Lin, L. K., Furuya‐Kanamori, L., Moore, C. E., Boeckel, T. P. V., Laxminarayan, R., & Yakob, L. (2023) · The Lancet Planetary Health · doi:10.1016/s2542-5196(23)00026-8 · Cited by 241 · see citing works
A conceptual framework for the environmental surveillance of antibiotics and antibiotic resistance
Huijbers, P. M. C., Flach, C.-F., & Larsson, D. G. J. (2019) · Environment International · doi:10.1016/j.envint.2019.05.074 · Cited by 236 · see citing works
Antibiotic resistance in urban aquatic environments: can it be controlled?
Manaia, C. M., Macedo, G., Fatta‐Kassinos, D., & Nunes, O. C. (2015) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-015-7202-0 · Cited by 235 · see citing works
The distribution of antibiotic use and its association with antibiotic resistance
Olesen, S. W., Barnett, M. L., MacFadden, D. R., Brownstein, J. S., Hernández–Dı́az, S., Lipsitch, M., & Grad, Y. H. (2018) · eLife · doi:10.7554/elife.39435 · Cited by 227 · see citing works
Global antibiotic use during the COVID-19 pandemic: analysis of pharmaceutical sales data from 71 countries, 2020–2022
Nandi, A., Pecetta, S., & Bloom, D. E. (2023) · EClinicalMedicine · doi:10.1016/j.eclinm.2023.101848 · Cited by 227 · see citing works
Systematic Review of Factors Associated with Antibiotic Prescribing for Respiratory Tract Infections
McKay, R., Mah, A., Law, M. R., McGrail, K. M., & Patrick, D. M. (2016) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00209-16 · Cited by 226 · see citing works
ECDC/EFSA/EMA first joint report on the integrated analysis of the consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals
(EFSA), E. F. S. A., & European Medicines Agency (EMA) (2015) · EFSA Journal · doi:10.2903/j.efsa.2015.4006 · Cited by 223 · see citing works
Burden of bacterial antimicrobial resistance in low-income and middle-income countries avertible by existing interventions: an evidence review and modelling analysis
Lewnard, J. A., Charani, E., Gleason, A., Hsu, L. Y., Khan, W. A., Karkey, A., Chandler, C. I. R., Mashe, T., Khan, E. A., Bulabula, A. N. H., et al. (2024) · The Lancet · doi:10.1016/s0140-6736(24)00862-6 · Cited by 220 · see citing works
Antimicrobial Resistance in the Food Chain: Trends, Mechanisms, Pathways, and Possible Regulation Strategies
Samtiya, M., Matthews, K. R., Dhewa, T., & Puniya, A. K. (2022) · Foods · doi:10.3390/foods11192966 · Cited by 217 · see citing works
The Contribution of Wastewater to the Transmission of Antimicrobial Resistance in the Environment: Implications of Mass Gathering Settings
Fouz, N., Pangesti, K. N. A., Yasir, M., Al‐Malki, A. L., Azhar, E. I., Hill-Cawthorne, G. A., & Ghany, M. A. E. (2020) · Tropical Medicine and Infectious Disease · doi:10.3390/tropicalmed5010033 · Cited by 208 · see citing works
Recommendations for antibacterial therapy in adults with COVID-19 – an evidence based guideline
Sieswerda, E., de Boer, M. G. J., Bonten, M. J. M., Boersma, W. G., Jonkers, R. E., Aleva, R. M., Kullberg, B. J., Schouten, J. A., van de Garde, E. M. W., Verheij, T. J., et al. (2020) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2020.09.041 · Cited by 199 · see citing works
Antimicrobial Usage in Animal Production: A Review of the Literature with a Focus on Low- and Middle-Income Countries
Cương, N. V., Padungtod, P., Thwaites, G. E., & Carrique-Mas, J. J. (2018) · Antibiotics · doi:10.3390/antibiotics7030075 · Cited by 187 · see citing works
Non-prescription dispensing of antibiotic agents among community drug retail outlets in Sub-Saharan African countries: a systematic review and meta-analysis
Belachew, S. A., Hall, L., & Selvey, L. A. (2021) · Antimicrobial Resistance and Infection Control · doi:10.1186/s13756-020-00880-w · Cited by 187 · see citing works
India's National Action Plan for antimicrobial resistance – An overview of the context, status, and way ahead
Ranjalkar, J., & Chandy, S. J. (2019) · Journal of Family Medicine and Primary Care · doi:10.4103/jfmpc.jfmpc_275_19 · Cited by 182 · see citing works
Antimicrobial resistance in leprosy: results of the first prospective open survey conducted by a WHO surveillance network for the period 2009–15
Cambau, E., Saunderson, P. R., Matsuoka, M., Cole, S. T., Kai, M., Suffys, P. N., Rosa, P. S., Williams, D. L., Gupta, U. D., Lavania, M., et al. (2018) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2018.02.022 · Cited by 180 · see citing works
Gender differences in antibiotic prescribing in the community: a systematic review and meta-analysis
Schröder, W., Sommer, H., Gladstone, B. P., Foschi, F., Hellman, J., Evengård, B., & Tacconelli, E. (2016) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkw054 · Cited by 179 · see citing works
Species Sensitivity to Toxic Substances: Evolution, Ecology and Applications
Spurgeon, D. J., Lahive, E., Robinson, A., Short, S., & Kille, P. (2020) · Frontiers in Environmental Science · doi:10.3389/fenvs.2020.588380 · Cited by 179 · see citing works
Antimicrobial stewardship in wound care: a Position Paper from the British Society for Antimicrobial Chemotherapy and European Wound Management Association
Lipsky, B. A., Dryden, M., Gottrup, F., Nathwani, D., Seaton, R. A., & Stryja, J. (2016) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkw287 · Cited by 178 · see citing works
Source tracking of antibiotic resistance genes in the environment — Challenges, progress, and prospects
Li, L.-G., Huang, Q., Yin, X., & Zhang, T. (2020) · Water Research · doi:10.1016/j.watres.2020.116127 · Cited by 178 · see citing works
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Authors: Bell, B. G., Schellevis, F., Stobberingh, E., Goossens, H., & Pringle, M.
Affiliations: University of Nottingham (GB)
Maastricht University (NL)
University of Antwerp (BE)
Corresponding author: Bell, Brian G
ORCID: Bell, Brian G
Goossens, Herman
Venue: BMC Infectious Diseases
Publisher: Springer Science and Business Media LLC
Published: 2014-01-09
Volume: 14
Issue: 1
Pages: 13-13
ISSN: 1471-2334 (ISSN-L)
DOI: 10.1186/1471-2334-14-13
PMC: PMC3897982
OpenAlex: W2064618548
Cited by: 1,262
References: 223
Citations by year: 2026: 56 · 2025: 91 · 2024: 151 · 2023: 151 · 2022: 149 · 2021: 156 · 2020: 158 · 2019: 105 · 2018: 93 · 2017: 60 · 2016: 50 · 2015: 27 · 2014: 13
FWCI: 7.04
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/2.0 (tdm)
Locations: BMC Infectious Diseases (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Research Publications (Maastricht University) (publishedVersion, cc-by)
Pure Amsterdam UMC (publishedVersion)
Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Research Publications (Maastricht University) (submittedVersion, other-oa)
Data Archiving and Networked Services (DANS) (submittedVersion)
Funders: European Commission (223083)
Topics: Life Sciences › Immunology and Microbiology › Applied Microbiology and Biotechnology › Antibiotic Use and Resistance
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
Physical Sciences › Environmental Science › Pollution › Pharmaceutical and Antibiotic Environmental Impacts
Keywords: antibiotic use, antibiotic resistance, community-acquired infections, antimicrobial resistance patterns, selection pressure, Southern Europe, regional variation in resistance
MeSH terms: Anti-Bacterial Agents, Drug Resistance, Microbial, Europe, Humans, Odds Ratio

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A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance

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