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Review

Anthropogenic Activities and the Problem of Antibiotic Resistance in Latin America: A Water Issue

by
Delfina C. Domínguez
1,*,
Luz María Chacón
2,* and
D’Janique Wallace
3,4
1
Clinical Laboratory Science Program, Department of Public Health Sciences, The University of Texas at El Paso, 500 W. University Ave. HSSN 420, El Paso, TX 79968, USA
2
Health Research Institute (INISA), University of Costa Rica, P.O. Box 11501-2060, San Pedro de Montes de Oca 11502, Costa Rica
3
Biology Department, El Paso Community College, P.O. Box 20500, El Paso, TX 79998, USA
4
Biological Sciences Department, The University of Texas at El Paso, 500 W University Ave., El Paso, TX 79968, USA
*
Authors to whom correspondence should be addressed.
Water 2021, 13(19), 2693; https://doi.org/10.3390/w13192693
Submission received: 31 July 2021 / Revised: 23 September 2021 / Accepted: 24 September 2021 / Published: 28 September 2021
(This article belongs to the Section Water Resources Management, Policy and Governance)
Browse Figures
Review Reports Versions Notes

Abstract

:
Antibiotics revolutionized modern medicine and have been an excellent tool to fight infections. However, their overuse and misuse in different human activities such as health care, food production and agriculture has resulted in a global antimicrobial resistance crisis. Some regions such as Latin America present a more complex scenario because of the lack of resources, systematic studies and legislation to control the use of antimicrobials, thus increasing the spread of antibiotic resistance. This review aims to summarize the state of environmental antibiotic resistance in Latin America, focusing on water resources. Three databases were searched to identify publications on antimicrobial resistance and anthropogenic activities in relation to natural and artificial water ecosystems. We found that antibiotic resistant bacteria, mainly against beta lactam antibiotics, have been reported in several Latin American countries, and that resistant bacteria as well as resistant genes can be isolated from a wide variety of aquatic environments, including drinking, surface, irrigation, sea and wastewater. It is urgent to establish policies and regulations for antibiotic use to prevent the increase of multi-drug resistant microorganisms in the environment.

1. Introduction

Antimicrobial resistance (AMR) is considered a major global health crisis faced by humankind. To combat this serious problem various initiatives have been created worldwide, including: the Transatlantic Taskforce on Antimicrobial Resistance (TATFAR), created in 2009 by Canada, European Union, Norway and the U.S.; the Global Antibiotic Resistance Partnership (GARP) created in 2009 to develop policy proposals on AMR in Low-income (LIC) and Middle-income countries (MIC); the Global Health Security Agenda (GHSA), a group of 70 countries to address global threats; the high level meeting on AMR by the United Nations in 2016; One Health Approach, which was designed to improve public health [1,2,3]; and the AMR Challenge 2018–2019, a yearlong effort to fight AMR among 350 organizations across the world [4,5]. Recent data by the CDC indicate that more than 2.8 million antibiotic resistance infections and 35,000 deaths occur each year in the U.S. [6]. In China, about 100,000 deaths are due to multi-drug resistant organisms (MDRO) [3,7]. At present, it is estimated that mortality rates due to AMR are 700,000 deaths annually [8]. The same report predicts that by 2050, the number of deaths may increase to 10 million per year.
Each year, the global consumption of antibiotics is estimated to be 70 billion standard units/year for humans [9]. Antibiotic usage is projected to increase by 67% within the next fifteen years [10]. The cost of AMR is not only monetary but also affects social activities and the workforce. The global economic impact is broad, affecting healthcare systems, healthcare providers, patients, pharmaceutical organizations and international policy [11]. The reduction of productivity can reach US $1.5 billion per year [7].
Global drivers for AMR include antibiotic overuse (humans and animals), antibiotic misuse, suboptimal therapeutic doses, inappropriate disposal of antimicrobials, and the use of antibiotics in agriculture, aquaculture and in cattle as prophylaxis and growth promoters for commercial purposes, which may contaminate rivers, streams, groundwater and soil [12,13,14].
The prolonged use of antimicrobials in livestock and aquaculture is of great concern, since the presence of antibiotic residues are found in the edible tissues of treated animals [15,16]. The use of antibiotics in animals varies significantly depending on the country. For example in Europe, North America and Japan, regulation of antibiotics is strict compared to developing countries where there is a lack of regulation and enforcement of the use of antibiotics [17]. However, the magnitude of the threat of AMR for public health from agriculture, livestock and aquaculture has not been quantified [15,17,18].
Dissemination of AMR occurs first through vertical transfer, bacterial mutations passed from bacterial parent cell to offspring, and second by horizontal transfer, which may include bacterial genetic elements such as plasmids and integrons or vectors such as humans and animals or vehicles such as water and food [14,19]. The mobility of antibiotic resistant genes (ARG) and the potential transmission to populations, animals and the environment is a major challenge that needs to be addressed [19]. Contamination hotspots include waste water treatment plants (WWTP), hospital sewage discharges and pharmaceutical industry waste [12,20].
AMR has affected all world countries, but the burden is disproportionally higher in low-income countries and middle-income countries. Challenges faced by Low- and Middle-income countries (LMIC) to combat AMR include political, economic, social, industrial, technological and environmental factors [21,22]. Reports from LMIC show that AMR is increasing and it is more common than in High income countries (HIC), not only in health care centers but also in the environment [19,23]. However, there is no conclusive evidence since this disparity may be due to sample bias, lack of standardized laboratory practices and underutilization of microbiological procedures [22,24].
Some of the factors favoring AMR in LMIC include population density, migration, and level of education, and infrastructure issues such as sanitation, poor hygiene, lack of potable water, untreated wastewater, illegal discharges and solid waste disposal. The low economy of these countries is the cause of lack of resources in medical centers, limited attention to prevention and infection control, and lack of microbiology laboratories and thus microbiology practices. Finally, poor governance contributes to lack of regulations in the antibiotic industry (forged antibiotics), lack of policies and overall ineffective health care centers [19,21,24,25].
In Latin America, MDRO are the leading cause of hospital acquired infections. According to surveillance data from the Latin American Network for antimicrobial Resistance Surveillance (ReLAVRA) an increased trend has been observed in carbapenem resistant bacteria since 2014 [26,27]. ReLAVRA is one of the oldest regional networks established by Pan American Health Organization (PAHO) and WHO in 1996 (PAHO, 2021). This network consists of 20 countries, including Argentina, Belize, Bolivia, Brazil, Chile, Colombia, Costa Rica, Cuba, Ecuador, El Salvador, Guatemala, Honduras, México, Nicaragua, Panamá, Paraguay, Perú, the Dominican Republic, Uruguay, and Venezuela. Each country is represented by a national reference laboratory (NRL). AMR data is collected each year to prioritize a number of pathogen-drug combinations [28].
In 2015, right after WHO launched the AMR Global Action Plan, PAHO developed five strategic actions to tackle AMR: (1) raising awareness, (2) surveillance and research, (3) prevention and control, (4) optimizing antibiotic usage, and (5) development of new diagnostics, new antimicrobials, vaccines, and interventions [27].
Patterns of antibiotic consumption have been monitored infrequently in Latin America. The assessment of antibiotic prescription/consumption has been challenging due to poor surveillance systems and unreliable data [29,30]. A study conducted on the utilization of antibiotics in eight Latin American counties from 1997–2007 showed that total antibiotic usage increased in Brazil, Perú, Uruguay and Venezuela. However, in México and Colombia, antibiotic consumption decreased [29]. Recent reports indicate that antibiotic utilization has increased during the past few years in Brazil, México, and Colombia [30,31,32,33]. The pharmacologic antibiotic group most commonly consumed varied in different countries but in general beta-lactams (penicillins and cephalosporins), quinolones, macrolides such as azithromycin and trimethoprim/sulfamethoxazole were the most reported [30,33,34,35]. Consumption and distribution of antibiotics varied greatly in different countries according to population concentration, accessibility and income [29,33,35]. Evaluating antibiotic consumption is challenging and very complex because it involves many variables; there are very few studies, information systems are not reliable and scarce [36]. However, knowledge about the patterns of antibiotic consumption is essential for the development of effective interventions and regulations.
Water is an essential natural resource for all ecosystems and a critical component for human health. However, over the past decades, several factors have dramatically affected the quality of natural (lakes, rivers, marine, groundwater) and artificial (wastewater, drinking water, artificial lakes and ponds) aquatic environments due to human activities [36,37] in Latin America and worldwide. Some of these human activities, such as urbanization, industrialization, farming and animal food production, have led to the dissemination of AMR [38,39,40,41]. Water has been recognized as an important vehicle of AMR but the public health impact attributed to the spread of AMR is poorly understood [42].
Some of the major problems favoring the spread of AMR in Latin American countries include great disparities in living conditions, ineffective healthcare systems, unreliable drug suppliers, poor sanitation and sewer disposal, and others [36]. Most of the studies conducted in Latin American countries in aquatic environments were performed in highly anthropogenic impacted environments such as rivers, lakes, and coastal waters which receive wastewater effluents; on the other hand, some of these water sources are used for irrigation and drinking water production. In these studies it is common to find phenotypic identification of resistant bacteria, ARG and mobile genetic elements reported [40,42,43].
The aim of this review is to analyze the anthropogenic activities that introduce MDRO to various aquatic environments in Latin America, as well as to investigate how these water bodies were utilized in different human activities such as drinking water production, vegetable irrigation, and aquaculture, among others. Here we present a summary of our findings and detailed information about the sources of resistant bacteria, identification procedures and antimicrobial resistant genes in different water sources. This information can be found in the Supplementary Materials.

2. Methods

Search Strategy: To understand the effects of human activities in natural and artificial aquatic ecosystems in Latin American countries we reviewed the most relevant studies related to antibiotic resistance, antibiotic use and how these water bodies were employed in communities or in populations. To include the maximum quantity of information a Google Scholar search was conducted in two languages, Spanish and English; in Spanish the words “bacterias resistentes” and “de aguas” was used, in the 2000–2020 timeframe, and 4560 entries were identified. All entries were checked by reviewing the title and abstract; only works published in indexed journals focusing on water ecosystems were included. Reviews published in Spanish were not included. For research studies published in English, in addition to Google Scholar, we searched additional databases including Science Direct and PubMed. A total of 23 Latin American countries were included: North America (México), Central America (Belize, Guatemala, Honduras, Nicaragua, El Salvador, Costa Rica, Panamá), South America (Argentina, Bolivia, Brazil, Chile, Colombia, Ecuador, French Guiana, Guyana, Paraguay, Perú, Suriname, Uruguay, Venezuela) and the Caribbean (Cuba, Dominican Republic, Haití). We configured the search as follows: “water” AND “resistant bacteria” AND “México” OR “Guatemala” OR “Honduras” OR “El Salvador” OR “Nicaragua” OR “Costa Rica” OR “Panamá” OR “Colombia” OR “Venezuela” OR “Peru” OR “Ecuador” OR “Bolivia” OR “Brazil” OR “Argentina” OR “Chile” OR “Uruguay” OR “Paraguay” OR “Cuba” OR “Haiti” OR “Dominican Republic” OR “Belize”, OR “Suriname” OR “French Guiana” OR “Guyana”, within the same timeframe (2000–2020). A total of 17,700 entries were recovered; the majority were either not related to antimicrobial resistance, water sources or the studies were not conducted in Latin American countries. All entries were checked reviewing the title and abstract. Only works published in indexed journals focusing on water ecosystems were included. Reviews in English were selected to write the introduction. Finally, 72 works were selected, 21 were published research studies in Spanish and 51 in English. Bacteria included Gram negative and Gram positive organisms found in natural and artificial water ecosystems. Susceptibility testing methodology and the level of resistance were evaluated from each report. Publications describing antimicrobial resistant determinants such as integrons and antimicrobial resistance genes were included.
Data Extraction: this was a descriptive study. Data obtained from included publications were exported to a database using a custom-made form. The database included:
  • Water sources, where the studied water samples were obtained, comprising rivers, and irrigation channels (surface water), seawater, and wastewater (treated and untreated).
  • Country where the studies were performed.
  • Anthropogenic activity affecting water bodies: agricultural activities, drinking water production, and wastewater discharges.
  • Reported antibiotic susceptibility analysis and antibiotic genetic marker detection methods.
  • Antibiotic resistance levels/Antibiotic resistance genes presence.
All these data are presented in the Supplementary Materials (Tables S1 and S2).
Data Analysis: We predicted that countries with high gross domestic product (GDP) were able to conduct more research studies; for this we ran a Spearman correlation between the number of published studies and the 2020 GDP [44]. The frequency of the most common antibiotic group types reported was evaluated. Additionally, we categorized the studies into two regions: Region 1 included North Latin America, Central America, and the Caribbean (NCC), and Region 2 included South America (SA). Statistical analysis and graphics were done using R program [45].

3. Results

A total of 72 publications were selected to review the studies conducted in Latin American countries on various aquatic environments, including natural and artificial water sources, in relation to antimicrobial resistance and its presence in human activities. Brazil was the country that published the most studies (31) [41,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74], followed by México (10) [37,75,76,77,78,79,80,81,82,83], Argentina (7) [84,85,86,87,88,89,90], Colombia (5) [91,92,93,94], Cuba (4) [95,96,97,98], Ecuador (4) [99,100,101,102], Chile (3) [103,104,105], Venezuela (3) [106,107,108], Costa Rica (2) [109,110], Bolivia (1) [111], Nicaragua (1) [112], and Perú (1) [113]. Figure 1 illustrates the number of published studies conducted by country. As we predicted, the Spearman correlation between the number of publications and the GDP was 0.90 (p = 0.0003593), which indicates that the more resources the country has, the more research is conducted.
Water sources studied in Latin America included: sea, surface, drinking, wastewater, irrigation, groundwater, estuarine, thermal and recreational waters as is shown in Supplementary Materials. In Figure 2 we present a summary of the water sources studied. Surface water was the most commonly studied (rivers and streams) (30), followed by wastewater (11), sea water (coastal water and recreational waters) (8), multiple water sources (for example river water and drinking water; recreational and irrigation water) (7), drinking water (6) lake water (3), and other, which included estuarine, thermal, groundwater and different recreational waters (7).
The anthropogenic activities related to water sources were reviewed to evaluate how different water bodies were utilized in different countries. We found very diverse usage of water sources by country. For example, 21 studies provided information on water bodies receiving treated/untreated wastewater; there were 11 reports on drinking water production; 10 studies reported on agricultural activities; hospital wastewater was discussed in 7 papers; finally, there were 14 studies reporting multiple human activities involved in a given water source, for example a lake that is used for irrigation, and also for drinking water production and recreational activities; other studies related to human activities (9) included studies with a great diversity of uses such as recreational, thermal waters, groundwater, and others. (Figure 3A).
In order to assess the work done according to research priorities per country, we categorized the studies into two regions: Region 1 included North Latin America, Central America and the Caribbean (NCC), and Region 2 included South America (SA). To avoid bias in the comparison of studies done per country we decided to use percentages (since Brazil had the highest number of studies in Latin America) and divided them by region. As shown in Figure 3B, 46% of water bodies receiving treated/untreated wastewater were reported by region 1, while 24% were reported by region 2; region 1 reported 18% for multiple human activities involving a given water source, while region 2 reported 20%; for drinking water production, region 1 reported 6% and region 2 18%; 18% of agricultural activities were reported by region 1 and 13% by region 2; studies on hospital wastewater were 6% in region 1 and 11% in region 2; 6% of other activities were reported from region 1 and 14% in region 2.
Bacterial antimicrobial resistance was studied phenotypically and genotypically. From the 72 research studies reviewed, 59 provided information on bacterial phenotypes. The most common antibiotics tested were cephalosporins, followed by aminoglycosides and penicillin. A summary of the different antibiotic groups tested is shown in Table 1. This Table also presents the percentage of studies that found resistant microorganisms in the aquatic environments in Region 1 (NCC) and Region 2 (SA). It is important to note that all the studies reported from NCC and SA found resistant microorganisms to carboxypenicillins, first generation cephalosporines, macrolides, and nitrofurans, since this groups of antibiotics have been used for a long time. Microorganisms resistant to carbapenems were more prevalent in SA than NCC. The most common technique used to assess antimicrobial susceptibility was the Kirby–Bauer disk diffusion method; other techniques used were the micro-broth dilution by automated analyzers such as Vitek® (bioMérieux, Inc., Marcy-l’Ètoile, France). Information about antimicrobial resistant genes was found in 27 publications. Of these, 23 reported the presence of ESBL genes, 7 reported quinolone resistant genes, 3 reported the presence of integrons and 12 reported the presence of other resistance genes. Most of these studies were done in bacterial isolates; a few studies were conducted using genomic DNA. Detailed information is presented in Table S2.

4. Discussion

There was a significant difference among Latin American countries’ publications. This may be related to the gross domestic product (GDP) of each country (p = 0.0003593). According to the International Monetary Fund, Brazil is listed at the top for GDP followed by Mexico and Argentina [114]. This correlates very well with the three countries that contributed the most publications. However, it could be possible that not all countries are interested in studying AMR or researching water ecosystems. No research studies were found for the following countries: Guatemala, Honduras, El Salvador, Panamá, Paraguay, Haiti, Dominican Republic, Belize, Suriname, Uruguay, French Guiana and Guyana. These findings are in agreement with those reported by Moreno-Switt (2020).
The most common studied water type was surface water. This water ecosystem has a wide variety of uses, which include irrigation, drinking water production, recreational activities and receivers of wastewaters. One big issue to be solved in Latin America is fecal contamination management. Only 37% of the LA countries have population access to improved sanitation facilities [115]. Another great concern is the great disparity in living conditions of communities in different countries. Rural communities that do not have sanitation facilities could disseminate MDRO by fecal material release to the environment; unfortunately, data about these populations is not available [115]. In many countries the availability of potable water data is unknown [115].
The second water source most commonly studied was wastewater. These ecosystems are of great concern since reports indicate that wastewaters are hot spots for AMR [42,116]. In addition, hospital wastewater effluents may play a role in dissemination of MDRO and ARG into the community and environment. For example, Spindler et al., 2012, reported the dissemination of carbapenem, cephalosporins resistant bacteria and the presence of integrons [58]. Resistance to several antibiotics (ESBL, 3rd generation cepholosporins, tetracyclines, quinolones and carbapenems) were reported by Picão et al., 2013 [60]. Wastewaters were studied intensely in South America [50,55,57,72]. Irrigation water has also been linked to the dissemination of AMR [82,84]. Contaminated irrigation water used in crop production has been of great concern since contaminated vegetables may lead to infections or other health consequences. Currently, the WHO Guidelines for Wastewater Use and Reuse do not include control of MDROs or antibiotic detection [117]. It is important to mention that only 50–60% of Latin America is connected to sewerage, and only 30% of domestic sewage is treated [118]. Due to the lack of financial resources in most countries, the management of wastewater is difficult.
Despite the significant threat that AMR represents worldwide and the urgent call for global action, many Latin American countries have not fully enforced policies to prevent the spread of AMR. Laws prohibiting over-the-counter antibiotic sales have been in place in several countries since 2010 [36,119]. However, effective surveillance programs and data regarding the impact on the decrease of antibiotic consumption are still not available [120]. In the veterinary and food production animal sectors, data on therapeutic and prophylactic use of antibiotics are still unavailable [121,122]. Chile, which is one of the countries leading the control of AMR in South America, has not yet established its National Plan to tackle AMR [123]. In summary, antibiotic use and AMR have been low on Latin American governments’ policy agendas. More comprehensive strategies, such as antibiotic stewardship programs, improvement of prescription quality, public health awareness and assessment of restrictive and structural interventions need to be instituted and enforced.
The interest and complexity of AMR research studies conducted in Latin American countries has increased during the last few years. At first, most of the AMR studies identified bacterial isolates phenotypically and tested antimicrobial susceptibility by diffusion methodology. However, most recent studies included advanced technologies such as automated analyzers, Vitek® and MALDI-TOF, and molecular identification by PCR [54,70,102]. Bacteria in these studies included a wide variety of genera and species. Gram negative bacilli were the most studied, specifically the Enterobacteriacea family and particularly E. coli and some non-fermenter bacteria such as Pseudomonas spp. and Acinetobacter spp. Supplementary Materials presents detailed information on the bacteria studied.

5. Conclusions

Despite the low number of reports on AMR and anthropogenic activities impacting water ecosystems in Latin American countries, information obtained in this study indicates that the spread of AMR is overwhelming. Latin American countries have diverse socioeconomic differences, and significant disparities exist in living conditions and lack of financial resources. Several factors contribute to the spread of AMR, such as lack of infrastructure and education, easy access to antibiotics and a lack of regulations. Development of public policies, public health awareness, better diagnostics and international surveillance may contribute to alleviating the serious AMR crisis.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/w13192693/s1, Table S1: Phenotypic evaluation of antimicrobial resistant bacteria collected from various aquatic environments in Latin America; Table S2: Antimicrobial Resistant Genes and mobile genetic elements reported from Latin American countries.

Author Contributions

Conceptualization and designed D.C.D. and L.M.C.; administration and coordination, D.C.D.; data analysis and interpretation D.C.D. and L.M.C., writing, editing D.C.D. and L.M.C.; literature review D.C.D., L.M.C.; L.M.C. and D.W., tables; L.M.C., D.C.D. references; L.M.C., figures. All authors have read and agreed to the published version of the manuscript.

Funding

This project was supported in part by the National Institute of General Medical Sciences of the National Institutes of Health under award numbers R25GM123928. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

The following abbreviations are used in this manuscript
AMRAntimicrobial Resistance
ARGAntimicrobial Resistant Genes
CDCCenters for Disease Control and Prevention
ESBLExtended Spectrum Beta Lactamases
GARP Global Antibiotic Resistance Partnership
GDPGross Domestic Product
GHSA Global Health Security Agenda
LMICLow- and Middle- Income Countries
LICLow- Income Countries
MALDI-TOFMatrix Assisted Laser Desorption Ionization Time of Flight
MICMiddle- Income Countries
MICMinimum Inhibitory concentration
MRDOMultidrug Resistant Organisms
PAHOPan American Health Organization
PCRPolymerase Chain Reaction
TATFARTransatlantic Taskforce on Antimicrobial Resistance
WHOWorld Health Organization
WWTPWastewater Treatment Plants

References

  1. Collignon, P.; McEwen, S. One Health—Its Importance in Helping to Better Control Antimicrobial Resistance. Trop. Med. Infect. Dis. 2019, 4, 22. [Google Scholar] [CrossRef] [Green Version]
  2. Nahrgang, S.; Nolte, E.; Rechel, B. The role of public health organizations in addressing antimicrobial resistance in Europe. Eur. J. Public Health 2018, 28. [Google Scholar] [CrossRef]
  3. World Health Organization. Global Antimicrobial Resistance and Use Surveillance System (GLASS). Available online: https://www.who.int/initiatives/glass (accessed on 23 September 2021).
  4. World Health Organization. Global Action Plan on Antimicrobial Resistance; World Health Organization (WHO), Ed.; World Health Organization: Geneva, Switerland, 2016; ISBN 9789241509763. [Google Scholar]
  5. Centers of Disease Control and Prevention. The ARM Challenge. Available online: https://www.cdc.gov/drugresistance/intl-activities/amr-challenge.html (accessed on 23 September 2021).
  6. Centers of Disease Control and Prevention. Antibiotic/Antimicrobial Resistance. Available online: https://www.cdc.gov/drugresistance/index.html (accessed on 23 September 2021).
  7. Martins, A.F.; Rabinowitz, P. The impact of antimicrobial resistance in the environment on public health. Future Microbiol. 2020, 15, 699–702. [Google Scholar] [CrossRef]
  8. O’Neil, J. Tackling Drug-Resistant Infections Globally: Final Report and Recommendations; Wellcome Trust: London, UK, 2016. [Google Scholar]
  9. Van Boeckel, T.P.; Gandra, S.; Ashok, A.; Caudron, Q.; Grenfell, B.T.; Levin, S.A.; Laxminarayan, R. Global antibiotic consumption 2000 to 2010: An analysis of national pharmaceutical sales data. Lancet Infect. Dis. 2014, 14, 742–750. [Google Scholar] [CrossRef]
  10. Center For Disease Dynamics Economics & Policy. The State of the World’s Antibiotics 2015; Cambridge University Press: Cambridge, UK, 2015. [Google Scholar]
  11. Ahmad, M.; Khan, A.U. Global economic impact of antibiotic resistance: A review. J. Glob. Antimicrob. Resist. 2019, 19, 313–316. [Google Scholar] [CrossRef]
  12. Pruden, A.; Pei, R.; Storteboom, H.; Carlson, K.H. Antibiotic Resistance Genes as Emerging Contaminants: Studies in Northern Colorado. Environ. Sci. Technol. 2006, 40, 7445–7450. [Google Scholar] [CrossRef]
  13. Baquero, F.; Martínez, J.-L.; Cantón, R. Antibiotics and antibiotic resistance in water environments. Curr. Opin. Biotechnol. 2008, 19, 260–265. [Google Scholar] [CrossRef]
  14. Domínguez, D.C.; Meza-Rodriguez, S.M. Development of antimicrobial resistance: Future challenges. In Pharmaceuticals and Personal Care Products: Waste Management and Treatment Technology; Butterworth-Heinemann: Oxford, UK, 2019; pp. 383–408. [Google Scholar]
  15. Magouras, I.; Carmo, L.P.; Stärk, K.D.C.; Schüpbach-Regula, G. Antimicrobial Usage and -Resistance in Livestock: Where Should We Focus? Front. Vet. Sci. 2017, 4, 148. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  16. Santos, L.; Ramos, F. Analytical strategies for the detection and quantification of antibiotic residues in aquaculture fishes: A review. Trends Food Sci. Technol. 2016, 52, 16–30. [Google Scholar] [CrossRef]
  17. Watts, J.; Schreier, H.; Lanska, L.; Hale, M. The Rising Tide of Antimicrobial Resistance in Aquaculture: Sources, Sinks and Solutions. Mar. Drugs 2017, 15, 158. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. Chang, Q.; Wang, W.; Regev-Yochay, G.; Lipsitch, M.; Hanage, W.P. Antibiotics in agriculture and the risk to human health: How worried should we be? Evol. Appl. 2015, 8, 240–247. [Google Scholar] [CrossRef] [Green Version]
  19. Vikesland, P.; Garner, E.; Gupta, S.; Kang, S.; Maile-Moskowitz, A.; Zhu, N. Differential Drivers of Antimicrobial Resistance across the World. Acc. Chem. Res. 2019, 52, 916–924. [Google Scholar] [CrossRef]
  20. Uyaguari-Díaz, M.I.; Croxen, M.A.; Luo, Z.; Cronin, K.I.; Chan, M.; Baticados, W.N.; Nesbitt, M.J.; Li, S.; Miller, K.M.; Dooley, D.; et al. Human Activity Determines the Presence of Integron-Associated and Antibiotic Resistance Genes in Southwestern British Columbia. Front. Microbiol. 2018, 9, 852. [Google Scholar] [CrossRef]
  21. Pokharel, S.; Raut, S.; Adhikari, B. Tackling antimicrobial resistance in low-income and middle-income countries. BMJ Glob. Heal. 2019, 4, e002104. [Google Scholar] [CrossRef]
  22. Vila, J. Update on Antibacterial Resistance in Low-Income Countries: Factors Favoring the Emergence of Resistance. Open Infect. Dis. J. 2010, 4, 38–54. [Google Scholar] [CrossRef]
  23. Pierce, J.; Apisarnthanarak, A.; Schellack, N.; Cornistein, W.; Maani, A.A.; Adnan, S.; Stevens, M.P. Global Antimicrobial Stewardship with a Focus on Low- and Middle-Income Countries: A position statement for the international society for infectious diseases. Int. J. Infect. Dis. 2020, 96, 621–629. [Google Scholar] [CrossRef] [PubMed]
  24. Gandra, S.; Alvarez-Uria, G.; Turner, P.; Joshi, J.; Limmathurotsakul, D.; van Doorn, H.R. Antimicrobial Resistance Surveillance in Low- and Middle-Income Countries: Progress and Challenges in Eight South Asian and Southeast Asian Countries. Clin. Microbiol. Rev. 2020, 33. [Google Scholar] [CrossRef]
  25. Collignon, P.; Beggs, J.J.; Walsh, T.R.; Gandra, S.; Laxminarayan, R. Anthropological and socioeconomic factors contributing to global antimicrobial resistance: A univariate and multivariable analysis. Lancet Planet. Health 2018, 2, e398–e405. [Google Scholar] [CrossRef]
  26. Gales, A.C.; Castanheira, M.; Jones, R.N.; Sader, H.S. Antimicrobial resistance among Gram-negative bacilli isolated from Latin America: Results from SENTRY Antimicrobial Surveillance Program (Latin America, 2008–2010). Diagn. Microbiol. Infect. Dis. 2012, 73, 354–360. [Google Scholar] [CrossRef]
  27. da Silva, J.B., Jr.; Espinal, M.; Ramón-Pardo, P. Antimicrobial resistance: Time for action. Rev. Panam. Salud Pública 2020, 44, 1. [Google Scholar] [CrossRef]
  28. Pan American Health Organization. Latin American Network for Antimicrobial Resistance Surveillance—ReLAVRA. Available online: https://www.paho.org/en/topics/antimicrobial-resistance/latin-american-network-antimicrobial-resistance-surveillance (accessed on 23 September 2021).
  29. Wirtz, V.J.; Dreser, A.; Gonzales, R. Trends in antibiotic utilization in eight Latin American countries, 1997–2007. Rev. Panam. Salud Publica/Pan Am. J. Public Health 2010, 27, 219–225. [Google Scholar] [CrossRef] [PubMed]
  30. Sánchez-Huesca, R.; Lerma, A.; Guzmán-Saldaña, R.M.E.; Lerma, C. Prevalence of Antibiotics Prescription and Assessment of Prescribed Daily Dose in Outpatients from Mexico City. Antibiotics 2020, 9, 38. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  31. Alvarez, C.; Gomez, C.; Montañez, A.; Ordoñez, K.; Bonilla, D.; Sussmann, O.; Group, A. Antibiotic Consumption from 2013 to 2015 at Colombian Hospitals of Third Level of Complexity. In Open Forum Infectious Diseases; Oxford University Press: Oxford, UK, 2016; Volume 3, p. 993. [Google Scholar] [CrossRef] [Green Version]
  32. Miranda-Novales, M.G.; Flores-Moreno, K.; López-Vidal, Y.; Rodríguez-Álvarez, M.; Solórzano-Santos, F.; Soto-Hernández, J.L.; Ponce de León-Rosales, S.; UNCAR Network. Antimicrobial resistance and antibiotic consumption in Mexican hospitals. Salud Publica Mex. 2019, 62, 42. [Google Scholar] [CrossRef] [PubMed]
  33. Neves e Castro, P.B.; da Silva Rodrigues, D.A.; Roeser, H.M.P.; da Fonseca Santiago, A.; de Cássia Franco Afonso, R.J. Antibiotic consumption in developing countries defies global commitments: An overview on Brazilian growth in consumption. Environ. Sci. Pollut. Res. 2020, 27, 21013–21020. [Google Scholar] [CrossRef]
  34. World Health Organization. WHO Report on Surveillance of Antibiotic Consumption: 2016–2018 Early Implementation; World Health Organization: Geneva, Switzerland, 2018. [Google Scholar]
  35. Peralta, N.; Camou, B.I.; Leszczuk, K.; Arcidiácono, D.; Lerena, R.G.; Herrera, P.; Cornistein, W.; Riera, F.; Cosgrove, S.E.; Fabre, V. Prevalence of hospital antibiotic use in Argentina, 2018. Infect. Control Hosp. Epidemiol. 2019, 40, 1301–1304. [Google Scholar] [CrossRef]
  36. Bonelli, R.R.; Moreira, B.M.; Picão, R.C. Antimicrobial resistance among Enterobacteriaceae in South America: History, current dissemination status and associated socioeconomic factors. Drug Resist. Updates 2014, 17, 24–36. [Google Scholar] [CrossRef]
  37. Canizalez-Roman, A.; Velazquez-Roman, J.; Valdez-Flores, M.A.; Flores-Villaseñor, H.; Vidal, J.E.; Muro-Amador, S.; Guadrón-Llanos, A.M.; Gonzalez-Nuñez, E.; Medina-Serrano, J.; Tapia-Pastrana, G.; et al. Detection of antimicrobial-resistance diarrheagenic Escherichia coli strains in surface water used to irrigate food products in the northwest of Mexico. Int. J. Food Microbiol. 2019, 304, 1–10. [Google Scholar] [CrossRef]
  38. Lozano-Muñoz, I.; Wacyk, J.; Kretschmer, C.; Vásquez-Martínez, Y.; Martin, M.C.-S. Antimicrobial resistance in Chilean marine-farmed salmon: Improving food safety through One Health. One Health 2021, 12, 100219. [Google Scholar] [CrossRef]
  39. Leite, B.; de Chaves, M.A.; Nunes, A.A.T.; Jank, L.; Corção, G. Antibiotic resistance in surface waters from a coastal lagoon of Southern Brazil under the impact of anthropogenic activities. Rev. Ambient. Agua. 2019, 14, 1. [Google Scholar] [CrossRef]
  40. Chamosa, L.S.; Álvarez, V.E.; Nardelli, M.; Quiroga, M.P.; Cassini, M.H.; Centrón, D. Lateral Antimicrobial Resistance Genetic Transfer is active in the open environment. Sci. Rep. 2017, 7, 513. [Google Scholar] [CrossRef]
  41. Coutinho, F.H.; Silveira, C.B.; Pinto, L.H.; Salloto, G.R.B.; Cardoso, A.M.; Martins, O.B.; Vieira, R.P.; Clementino, M.M. Antibiotic Resistance is Widespread in Urban Aquatic Environments of Rio de Janeiro, Brazil. Microb. Ecol. 2014, 68, 441–452. [Google Scholar] [CrossRef]
  42. Moreno-Switt, A.I.; Rivera, D.; Caipo, M.L.; Nowell, D.C.; Adell, A.D. Antimicrobial resistance in water in Latin America and the Caribbean: Available Research and Gaps. Front. Vet. Sci. 2020, 7, 546. [Google Scholar] [CrossRef]
  43. Overbey, K.N.; Hatcher, S.M.; Stewart, J.R. Water quality and antibiotic resistance at beaches of the Galápagos Islands. Front. Environ. Sci. 2015, 3, 64. [Google Scholar] [CrossRef] [Green Version]
  44. The World Bank. GDP (Curren US$). Available online: https://data.worldbank.org/indicator/NY.GDP.MKTP.CD?view=map (accessed on 23 September 2021).
  45. R Core Team. R: A Language and Environment for Statistical Computing; R Core Team: Vienna, Austria, 2019; Available online: https://www.R-project.org/ (accessed on 23 September 2021).
  46. Bartley, P.S.; Domitrovic, T.N.; Moretto, V.T.; Santos, C.S.; Ponce-Terashima, R.; Reis, M.G.; Barbosa, L.M.; Blanton, R.E.; Bonomo, R.A.; Perez, F. Antibiotic resistance in enterobacteriaceae from surface waters in Urban Brazil highlights the risks of poor sanitation. Am. J. Trop. Med. Hyg. 2019, 100, 1369–1377. [Google Scholar] [CrossRef]
  47. De Oliveira, A.J.F.C.; Watanabe Pinhata, J.M. Antimicrobial resistance and species composition of Enterococcus spp. isolated from waters and sands of marine recreational beaches in Southeastern Brazil. Water Res. 2008, 42, 2242–2250. [Google Scholar] [CrossRef]
  48. Basso, A.P.; Martins, P.D.; Nachtigall, G.; van der Sand, S.; de Moura, T.M.; Frazzon, A.P.G. Antibiotic resistance and enterotoxin genes in staphylococcus sp. Isolates from polluted water in southern Brazil. An. Acad. Bras. Cienc. 2014, 86, 1813–1820. [Google Scholar] [CrossRef] [Green Version]
  49. Turano, H.; Gomes, F.; Medeiros, M.; Oliveira, S.; Fontes, L.C.; Sato, M.I.Z.; Lincopan, N. Presence of high-risk clones of OXA-23-producing Acinetobacter baumannii (ST79) and SPM-1-producing Pseudomonas aeruginosa (ST277) in environmental water samples in Brazil. Diagn. Microbiol. Infect. Dis. 2016, 86, 80–82. [Google Scholar] [CrossRef] [PubMed]
  50. Chagas, T.P.G.; Seki, L.M.; Cury, J.C.; Oliveira, J.A.L.; Dávila, A.M.R.; Silva, D.M.; Asensi, M.D. Multiresistance, beta-lactamase-encoding genes and bacterial diversity in hospital wastewater in Rio de Janeiro, Brazil. J. Appl. Microbiol. 2011, 111, 572–581. [Google Scholar] [CrossRef] [PubMed]
  51. Edirsana, M.R.C.; Renata, A.C.; Alberto, J.G.A.; Ftima, C.T.C.; Silvano, P.P.; Oscarina, V.S.; Regine, H.S.F.V. Multiple antibiotic-resistance of Enterococcus isolated from coastal water near an outfall in Brazil. Afr. J. Microbiol. Res. 2014, 8, 1825–1831. [Google Scholar] [CrossRef] [Green Version]
  52. Miranda, C.C.; de Filippis, I.; Pinto, L.H.; Coelho-Souza, T.; Bianco, K.; Cacci, L.C.; Picão, R.C.; Clementino, M.M. Genotypic characteristics of multidrug-resistant Pseudomonas aeruginosa from hospital wastewater treatment plant in Rio de Janeiro, Brazil. J. Appl. Microbiol. 2015, 118, 1276–1286. [Google Scholar] [CrossRef]
  53. Dos Rocha, R.S.; de Sousa, O.V.; dos Vieira, R.H.S.F. Multidrug-resistant Vibrio associated with an estuary affected by shrimp farming in Northeastern Brazil. Mar. Pollut. Bull. 2016, 105, 337–340. [Google Scholar] [CrossRef]
  54. Conte, D.; Palmeiro, J.K.; da Silva Nogueira, K.; de Lima, T.M.R.; Cardoso, M.A.; Pontarolo, R.; Degaut Pontes, F.L.; Dalla-Costa, L.M. Characterization of CTX-M enzymes, quinolone resistance determinants, and antimicrobial residues from hospital sewage, wastewater treatment plant, and river water. Ecotoxicol. Environ. Saf. 2017, 136, 62–69. [Google Scholar] [CrossRef]
  55. Oliveira, L.G.; Ferreira, L.G.R.; Nascimento, A.M.A.; Reis, M.D.P.; Dias, M.F.; Lima, W.G.; Paiva, M.C. Antibiotic resistance profile and occurrence of Amp C between Pseudomonas aeruginosa isolated from a domestic full-scale WWTP in southeast Brazil. Water Sci. Technol. 2018, 108–114. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. Freitas, D.Y.; Araújo, S.; Folador, A.R.C.; Ramos, R.T.J.; Azevedo, J.S.N.; Tacão, M.; Silva, A.; Henriques, I.; Baraúna, R.A. Extended spectrum beta-lactamase-producing gram-negative bacteria recovered from an amazonian lake near the city of Belém, Brazil. Front. Microbiol. 2019, 10, 364. [Google Scholar] [CrossRef] [Green Version]
  57. Zagui, G.S.; de Andrade, L.N.; Moreira, N.C.; Silva, T.V.; Machado, G.P.; da Costa Darini, A.L.; Segura-Muñoz, S.I. Gram-negative bacteria carrying β-lactamase encoding genes in hospital and urban wastewater in Brazil. Environ. Monit. Assess. 2020, 192. [Google Scholar] [CrossRef]
  58. Spindler, A.; Otton, L.M.; Fuentefria, D.B.; Corção, G. Beta-lactams resistance and presence of class 1 integron in Pseudomonas spp. isolated from untreated hospital effluents in Brazil. Antonie Leeuwenhoek 2012, 102, 73–81. [Google Scholar] [CrossRef] [PubMed]
  59. De Souza, M.; da Pinto, F.G.S.; Fruet, T.K.; Piana, P.A.; de Moura, A.C. Water quality indicators for environmental and resistance profile of Escherichia coli strains isolated in Rio Cascavel, Paraná, Brazil. Eng. Agrícola 2014, 34, 352–362. [Google Scholar] [CrossRef] [Green Version]
  60. Picão, R.C.; Cardoso, J.P.; Campana, E.H.; Nicoletti, A.G.; Petrolini, F.V.B.; Assis, D.M.; Juliano, L.; Gales, A.C. The route of antimicrobial resistance from the hospital effluent to the environment: Focus on the occurrence of KPC-producing Aeromonas spp. and Enterobacteriaceae in sewage. Diagn. Microbiol. Infect. Dis. 2013, 76, 80–85. [Google Scholar] [CrossRef] [Green Version]
  61. Zanetti, M.O.; Martins, V.V.; Pitondo-Silva, A.; Stehling, E.G. Antimicrobial resistance, plasmids and class 1 and 2 integrons occurring in Pseudomonas aeruginosa isolated from Brazilian aquatic environments. Water Sci. Technol. 2013, 67, 1144–1149. [Google Scholar] [CrossRef]
  62. Giowanella, M.; Bozza, A.; do Rocio Dalzoto, P.; Dionísio, J.A.; Andraus, S.; Guimarães, E.L.G.; Pimentel, I.C. Microbiological quality of water from the rivers of Curitiba, Paraná State, Brazil, and the susceptibility to antimicrobial drugs and pathogenicity of Escherichia coli. Environ. Monit. Assess. 2015, 187. [Google Scholar] [CrossRef]
  63. Falcão, J.P.; Brocchi, M.; Proença-Módena, J.L.; Acrani, G.O.; Corrêa, E.F.; Falcão, D.P. Virulence characteristics and epidemiology of Yersinia enterocolitica and Yersiniae other than Y. pseudotuberculosis and Y. pestis isolated from water and sewage. J. Appl. Microbiol. 2004, 96, 1230–1236. [Google Scholar] [CrossRef] [Green Version]
  64. Gomes Freitas, D.; Silva, R.D.R.; Bataus, L.A.M.; Barbosa, M.S.; da Silva Bitencourt Braga, C.A.; Carneiro, L.C. Bacteriological water quality in school’s drinking fountains and detection antibiotic resistance genes. Ann. Clin. Microbiol. Antimicrob. 2017, 16, 1–5. [Google Scholar] [CrossRef] [Green Version]
  65. Lima-Bittencourt, C.I.; Cursino, L.; Gonçalves-Dornelas, H.; Pontes, D.S.; Nardi, R.M.D.; Callisto, M.; Chartone-Souza, E.; Nascimento, A.M.A. Multiple antimicrobial resistance in Enterobacteriaceae isolates from pristine freshwater. Genet. Mol. Res. 2007, 6, 510–521. [Google Scholar]
  66. Abraham, W.R.; Macedo, A.J.; Gomes, L.H.; Tavares, F.C.A. Occurrence and resistance of pathogenic bacteria along the Tietê River downstream of São Paulo in Brazil. Clean-Soil Air Water 2007, 35, 339–347. [Google Scholar] [CrossRef]
  67. Canal, N.; Meneghetti, K.L.; De Almeida, C.P.; Da Rosa Bastos, M.; Otton, L.M.; Corção, G. Characterization of the variable region in the class 1 integron of antimicrobial-resistant Escherichia coli isolated from surface water. Braz. J. Microbiol. 2016, 47, 337–344. [Google Scholar] [CrossRef] [Green Version]
  68. De Araujo, C.F.M.; Silva, D.M.; Carneiro, M.T.; Ribeiro, S.; Fontana-Maurell, M.; Alvarez, P.; Asensi, M.D.; Zahner, V.; Carvalho-Assef, A.P.D. Detection of Carbapenemase Genes in Aquatic Environments in Rio de Janeiro, Brazil. Antimicrob. Agents Chemother. 2016, 60, 4380–4383. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  69. Furlan, J.P.R.; Stehling, E.G. Detection of β-lactamase encoding genes in feces, soil and water from a Brazilian pig farm. Environ. Monit. Assess. 2018, 190. [Google Scholar] [CrossRef] [PubMed]
  70. Sanchez, D.G.; de Melo, F.M.; Savazzi, E.A.; Stehling, E.G. Detection of different β-lactamases encoding genes, including bla NDM, and plasmid-mediated quinolone resistance genes in different water sources from Brazil. Environ. Monit. Assess. 2018, 190. [Google Scholar] [CrossRef]
  71. Gonçalves, V.D.; Meirelles-Pereira, F.; Cataldo, M.; de Fonseca, B.O.; Nogueira, B.A.; Olivella, J.G.B.; de Esteves, F.A.; Mattos-Guaraldi, A.L.; de Andrade, A.F.B.; Bello, A.R.; et al. Detection of multidrug-resistant Enterobacteria isolated from river waters flowing to Guanabara Bay (Rio de Janeiro, Brazil) and from clinical samples of hospital origin. Biomedica 2019, 39, 135–149. [Google Scholar] [CrossRef]
  72. Arsand, J.B.; Hoff, R.B.; Jank, L.; Bussamara, R.; Dallegrave, A.; Bento, F.M.; Kmetzsch, L.; Falção, D.A.; do Carmo Ruaro Peralba, M.; de Araujo Gomes, A.; et al. Presence of antibiotic resistance genes and its association with antibiotic occurrence in Dilúvio River in southern Brazil. Sci. Total Environ. 2020, 738, 139781. [Google Scholar] [CrossRef]
  73. Fernandes, M.R.; Sellera, F.P.; Moura, Q.; Esposito, F.; Sabino, C.P.; Lincopan, N. Identification and genomic features of halotolerant extended-spectrum-β-lactamase (CTX-M)-producing Escherichia coli in urban-impacted coastal waters, Southeast Brazil. Mar. Pollut. Bull. 2020, 150, 110689. [Google Scholar] [CrossRef]
  74. Fuentefria, D.B.; Ferreira, A.E.; Gräf, T.; Corção, G. Spread of metallo-β-lactamases: Screening reveals the presence of a blaspm-1 gene in hospital sewage in southern Brazil. Braz. J. Microbiol. 2009, 40, 82–85. [Google Scholar] [CrossRef] [Green Version]
  75. Gutierrez, O.; Navarro, L.; Loeza, P.; Del Río, O.; Jiménez, R. Perfiles de resistencia a antibióticos y metales pesados en Pseudomonas aeruginosa potencialmente patógenas aisladas de agua de uso agrícola Antibiotic and heavy metal resistance profiles in potentially pathogenic Pseudom. Rev. Electrónica Nov. Sci. 2017, 9, 97–112. [Google Scholar]
  76. Correa-Basurto, A.; Peña-Betancourt, M.T.N.-C.S.D. Bacterias heterótrofas aisladas del lago de los Reyes Aztecas ( Tlahuac ) y su resistencia a diferentes antibióticos. Rev. Latinoam. Recur. Nat. 2007, 3, 84–89. [Google Scholar]
  77. Cruz-Leyva, M.C.; González-de la Cruz, J.U.; Debelis Urbina, V.C.; Álvarez González, C.A.; Cuenca-Soria, C.A. Resistencia De Salmonella Spp A Antibióticos Y Fluctuación Fisicoquímica Del Agua A Nivel Espacial En La Cuenca Media Del Río Usumacinta, México. Eur. Sci. J. ESJ 2020, 16, 43–56. [Google Scholar] [CrossRef]
  78. Martínez-Orgániz, A.; Garza-Ramos, U.; Sampedro-Rosas, M.L.; González-González, J.; Nava-Faustino, G.; Toribio Jiménez, J. Patotipos y resistencia aantibióticos de Escherichia coli en agua residual. Rev. Int. Contam. Ambient. 2020, 36, 957–966. [Google Scholar] [CrossRef]
  79. Delgado-Gardea, M.C.E.; Tamez-Guerra, P.; Gomez-Flores, R.; de la Serna, F.J.Z.D.; Eroza-de la Vega, G.; Nevárez-Moorillón, G.V.; Pérez-Recoder, M.C.; Sánchez-Ramírez, B.; González-Horta, M.D.C.; Infante-Ramírez, R. Multidrug-resistant bacteria isolated from surface water in Bassaseachic Falls National Park, Mexico. Int. J. Environ. Res. Public Health 2016, 13, 597. [Google Scholar] [CrossRef] [Green Version]
  80. Mondragón, V.A.; Llamas-Pérez, D.F.; González-Guzmán, G.E.; Márquez-González, A.R.; Padilla-Noriega, R.; Durán-Avelar, M.d.J.; Franco, B. Identification of Enterococcus faecalis bacteria resistant to heavy metals and antibiotics in surface waters of the Mololoa River in Tepic, Nayarit, Mexico. Environ. Monit. Assess. 2011, 183, 329–340. [Google Scholar] [CrossRef] [PubMed]
  81. Ramírez Castillo, F.Y.; Avelar González, F.J.; Garneau, P.; Díaz, F.M.; Guerrero Barrera, A.L.; Harel, J. Presence of multi-drug resistant pathogenic Escherichia coli in the San Pedro River located in the State of Aguascalientes, Mexico. Front. Microbiol. 2013, 4, 147. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  82. Rosas, I.; Salinas, E.; Martínez, L.; Cruz-Còrdova, A.; Gonzàlez-Pedrajo, B.; Espinosa, N.; Amábile-Cuevas, C.F. Characterization of Escherichia coli isolates from an urban lake receiving water from a wastewater treatment plant in Mexico city: Fecal pollution and antibiotic resistance. Curr. Microbiol. 2015, 71, 490–495. [Google Scholar] [CrossRef] [PubMed]
  83. Lugo-Melchor, Y.; Quiñones, B.; Amézquita-López, B.A.; León-Félix, J.; García-Estrada, R.; Chaidez, C. Characterization of tetracycline resistance in salmonella enterica strains recovered from irrigation water in the culiacan valley, Mexico. Microb. Drug Resist. 2010, 16, 185–190. [Google Scholar] [CrossRef] [Green Version]
  84. Nuñez, L.; Tornello, C.; Puentes, N.; Moretton, J. Bacterias resistentes a antibióticos en aguas grises como agentes de riesgo sanitario. Rev. Ambient. Agua 2012, 7, 235–243. [Google Scholar] [CrossRef]
  85. Muñoz, A.V.; Pucci, O.H.; Pucci, G.N. Cepas bacterianas resistentes a ampicilina, cefotaxima, ceftazidima, clindamicina, gentamicina, imipenem, meropenem y vancomicina, aisladas de agua de mar en la ciudad de Comodoro Rivadavia (Argentina). Hig. Sanid. Ambient. 2014, 14, 1253–1257. [Google Scholar]
  86. Baldini, M.; Selzer, P. Patrones de resistencia a antibióticos de enterococos aislados de aguas estuarinas. Rev. Argent. Microbiol. 2008, 40, 48–51. [Google Scholar]
  87. Balcaza, J.A.; Kurz, I.; Macin, C.I.; Mosquera, M.S.; Sandi, A.; López, D.; Leyes, S.R.; Lösch, L.S.; Merino, L.A. Resistencia a fosfomicina, tigeciclina y colistina en enterobacterias provenientes de ambientes acuáticos del Chaco, Argentina. Rev. Cienc. Tecnol. 2020, 96–100. [Google Scholar] [CrossRef]
  88. Bianchi, V.; Varela, P.; Flores, D.; Ruta, N.; Andes, J.D.L.; Bianchi, V.; Varela, P.; Flores, D.; Durando, P. Evaluation of Escherichia coli resistant to antibiotics as a bioindicator species of fecal pollution in water and fishes in the lower basin of the San Juan River. Nat. Neotrop. 2014, 45, 45–69. [Google Scholar]
  89. Lösch, L.S.; Merino, L.A. Susceptibilidad antimicrobiana de aislamientos de Escherichia coli provenientes de diversas fuentes de agua del Chaco (Argentina). Hig. Sanid. Ambient. 2012, 12, 913–917. [Google Scholar]
  90. Lösch, L. Occurrence of antimicrobial-resistant Enterobacteriaceae in water from different sources in a subtropical region of Argentina. Ambient. Agua 2008, 3, 28–36. [Google Scholar] [CrossRef] [Green Version]
  91. Pulido Beltrán, J.A.; Rodríguez, X.A.; Méndez, I.A. Perfil de resistencia antimicrobiana en bacilos Gram negativos no fermentadores aislados en fuentes hídricas. Rev. Médica Risaralda 2017, 23, 38–42. [Google Scholar] [CrossRef]
  92. Tamayo Morales, L.; Husserl Orjuela, J. Cuantificación de cepas de Salmonella sp. resistentes a antibióticos en muestras de agua del Río Bogotá. In Proceedings of the IAMB201320, Los Andes, Colombia, 26–28 September 2013. [Google Scholar]
  93. Vivas, M.C.; Caicedo, L.D.; Castillo, J.E. Occurrence of β-Lactamase-Producing Gram-Negative Bacterial Isolates in Water Sources in Cali City, Colombia. Int. J. Microbiol. 2019, 2019, 1375060. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  94. Rodríguez, E.A.; Garzón, L.M.; Gómez, I.D.; Jiménez, J.N. Multidrug resistance and diversity of resistance profiles in carbapenem-resistant Gram-negative bacilli throughout a wastewater treatment plant in Colombia. J. Glob. Antimicrob. Resist. 2020, 22, 358–366. [Google Scholar] [CrossRef]
  95. Díaz, R.D.L.A.J.; Pita, M.T.S.; Weng, Z.; Rubalcaba, S.C.; González, M.I.; Rosa, O.E.D.; Caridad, M.; Salazar, R. Sensibilidad antimicrobiana en bacterias de origen ambiental. Hig. Sanid. Ambient. 2006, 6, 150–159. [Google Scholar]
  96. Martínez, A.; Cruz, M.; Veranes, O.; Carballo, M.E.; Salgado, I.; Olivares, S.; Lima, L.; Rodríguez, D. Resistencia a antibióticos y a metales pesados en bacterias aisladas del río Almendares. Rev. CENIC Cienc. Biológicas 2010, 41, 1–10. [Google Scholar]
  97. Romeu Álvarez, B.; Salazar Jiménez, P.; Lugo Moya, D.; Rojas Hernández, N.M.; Eslava Campos, C.A. Susceptibilidad antimicrobiana de aislamientos de Escherichia coli procedentes de ecosistemas dulceacuícolas. Rev. Cubana Med. Trop. 2012, 64, 132–141. (In Spanish) [Google Scholar]
  98. Arpajón-Peña, Y.; Doval-García, R.; Hernández-Carretero, J.G.; Pérez-Cosme, M.; Llano-González, Y. La antibiótico-resistencia de bacterias de importancia clínica aisladas del río Almendares, Cuba, abordada como problema de salud ecosistémica. Univ. Salud 2014, 16, 58–66. [Google Scholar]
  99. Vargas, E.; Escobar, S.; Espinoza, C.; Fierro, A.; Araque, J.; Andueza, F. Perfiles de susceptibilidad antimicrobiana en bacterias aisladas del agua de consumo en la ciudad de Riobamba, provincia de Chimborazo, Ecuador. Vitae 2016, 23, S25–S26. [Google Scholar]
  100. González, M.; Viteri, F.; Villacís, L.; Escobar, J.; Araujo, L.; González, A.; Medina, G.; Araque, J. Perfiles de susceptibilidad a los antibioticos en cepas del genero Bacillus aisladas de ambientes acuáticos estremos del Ecuador. An. RANF 2021, 87, 27–34. [Google Scholar] [CrossRef]
  101. Andueza, F.; Albuja, A.; Arguelles, P.; Escobar, S.; Espinoza, C.; Araque, J.; Medina, G. Resistencia antimicrobiana en cepas de Pseudomonas aeruginosa aisladas de aguas termales de la provincia del Chimborazo, Ecuador. An. RANF 2015, 81, 158–163. [Google Scholar]
  102. Ortega-Paredes, D.; Barba, P.; Mena-López, S.; Espinel, N.; Crespo, V.; Zurita, J. High quantities of multidrug-resistant Escherichia coli are present in the Machángara urban river in Quito, Ecuador. J. Water Health 2020, 18, 67–76. [Google Scholar] [CrossRef]
  103. Silva, J.; Castillo, G.; Callejas, L.; López, H.; Olmos, J. Frequency of transferable multiple antibiotic resistance amongst coliform bacteria isolated from a treated sewage effluent in Antofagasta, Chile. Electron. J. Biotechnol. 2006, 9, 533–540. [Google Scholar] [CrossRef] [Green Version]
  104. Martínez, M.C.; Retamal, P.; Rojas-Aedo, J.F.; Fernández, J.; Fernández, A.; Lapierre, L. Multidrug-Resistant Outbreak-Associated Salmonella Strains in Irrigation Water from the Metropolitan Region, Chile. Zoonoses Public Health 2017, 64, 299–304. [Google Scholar] [CrossRef]
  105. Tomova, A.; Ivanova, L.; Buschmann, A.H.; Rioseco, M.L.; Kalsi, R.K.; Godfrey, H.P.; Cabello, F.C. Antimicrobial resistance genes in marine bacteria and human uropathogenic Escherichia coli from a region of intensive aquaculture. Environ. Microbiol. Rep. 2015, 7, 803–809. [Google Scholar] [CrossRef]
  106. Rojas Pirela, M.L.; Botello Suárez, W.A.; Ball Vargas, M.M. Antibiotic- and heavy-metal resistance in bacteria isolated from deep subsurface in El Callao region, Venezuela. Rev. Colomb. Biotechnol. 2014, 16, 141–149. [Google Scholar] [CrossRef]
  107. Correa Rivas, K.; Bravo Torrealba, M.V.; Silva Alvarado, R.A.; Montiel, M. Susceptibilidad a antibióticos de Pseudomonas aeruginosa aislada de agua de consumo humano de la comunidad Santa Rosa de Agua, Maracaibo, estado Zulia. Rev. Soc. Venez. Microbiol. 2015, 35, 83–88. [Google Scholar]
  108. Fernández-Delgado, M.; Suárez, P. Multiple antibiotic resistances of enteric bacteria isolated from recreational coastal waters and oysters of the Caribbean Sea. Ann. Microbiol. 2009, 59, 409–414. [Google Scholar] [CrossRef]
  109. Rojas-Alfaro, R.; Umaña-Castro, R.; Rojas-Campos, N.; Vargas-Montero, M. Primer reporte de bacterias y dinoflagelados marinos luminiscentes del Parque Nacional Isla del Coco, Costa Rica. Rev. Biol. Trop. 2020, 68, S213–S224. [Google Scholar] [CrossRef]
  110. Tzoc, E.; Arias, M.L.; Valiente, C. Efecto de las aguas residuales hospitalarias sobre los patrones de resistencia a los antibióticos de Escherichia coli y Aeromonas sp. Rev. Biomédica 2004, 15, 165–172. [Google Scholar] [CrossRef] [Green Version]
  111. Guzman-Otazo, J.; Gonzales-Siles, L.; Poma, V.; Bengtsson-Palme, J.; Thorell, K.; Flach, C.-F.; Iñiguez, V.; Sjöling, Å. Diarrheal bacterial pathogens and multi-resistant enterobacteria in the Choqueyapu River in La Paz, Bolivia. PLoS ONE 2019, 14, e0210735. [Google Scholar] [CrossRef]
  112. Amaya, E.; Reyes, D.; Paniagua, M.; Calderón, S.; Rashid, M.U.; Colque, P.; Kühn, I.; Möllby, R.; Weintraub, A.; Nord, C.E. Antibiotic resistance patterns of Escherichia coli isolates from different aquatic environmental sources in León, Nicaragua. Clin. Microbiol. Infect. 2012, 18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  113. Larson, A.; Hartinger, S.M.; Riveros, M.; Salmon-Mulanovich, G.; Hattendorf, J.; Verastegui, H.; Huaylinos, M.L.; Mäusezahl, D. Antibiotic-resistant Escherichia coli in drinking water samples from rural andean households in Cajamarca, Peru. Am. J. Trop. Med. Hyg. 2019, 100, 1363–1368. [Google Scholar] [CrossRef]
  114. International Monetary Fund. Report for Selected Countries and Subjects. Available online: https://www.imf.org/en/Publications/SPROLLs/world-economic-outlook-databases#sort=%40imfdatedescending (accessed on 23 September 2021).
  115. Pan American Health Organization. Health Situation in the Americas. Core Indicators 2018; Pan American Health Organization: Washington, DC, USA, 2018. [Google Scholar]
  116. Ramírez-Castillo, F.Y.; Harel, J.; Moreno-Flores, A.C.; Loera-Muro, A.; Guerrero-Barrera, A.L.; Avelar-González, F.J. Antimicrobial resistance: The role of aquatic environments. Int. J. Curr. Res. Acad. Rev. 2014, 2, 231–243. [Google Scholar]
  117. World Health Organization. WHO Guidelines for Safe Use of Wasteater, Excreta and Greywater; World Health Organization: Geneva, Switzerland, 2006; Available online: https://www.who.int/water_sanitation_health/publications/gsuweg4/en/ (accessed on 23 September 2021).
  118. Rodríguez, D. Investing in Wastewater in Latin America Can Pay Off. 2017. Available online: https://blogs.worldbank.org/water/how-can-we-make-wastewater-investments-sustainable-latin-america (accessed on 23 September 2021).
  119. Deser, A.; Vázquez-Vélez, E.; Treviño, S.; Wirtz, V. Regulation of antibiotic sales in Mexico: An analysis of printed media coverage and stakeholder participation. BMC Public Health 2012, 12, 1051. [Google Scholar] [CrossRef] [Green Version]
  120. Pan American Health Organization. Latin American Countries Advance in the Surveillance of Antimicrobial Consumption; Pan American Health Organization: Washington, DC, USA, 2021; Available online: https://www.paho.org/en/news/21-4-2021-latin-american-countries-advance-surveillance-antimicrobial-consumption (accessed on 23 September 2021).
  121. Zaidi, M.; Dreser, A.; Figueroa, I.M. A collaborative initiative for the containment of antimicrobial resistance in Mexico. Zoonoses Public Health. 2015, 62 (Suppl. 1), 52–57. [Google Scholar] [CrossRef]
  122. Rabello, R.; Bonelli, R.; Penna, B.; Alburquerque, J.; Souza, R.; Cerqueira, A. Antimicrobial resistance in farm animals in Brazil: An update overview. Animals 2020, 10, 552. [Google Scholar] [CrossRef] [Green Version]
  123. Cabrera-Pardo, J.; Lood, R.; Udekwu, K.; Gonzalez-Rocha, G.; Munita, J.; Järhult, J.; Opazo-Capurro, A. A One Health—One World initiative to control antibiotic resistance: A Chile–Sweden collaboration. One Health 2019, 8, 100100. [Google Scholar] [CrossRef]
Water 13 02693 g001 550
Figure 1. Latin American countries studying aquatic ecosystems. Brazil is the leading country with 31 publications, followed by México 10, Argentina, 7 Colombia 5, Cuba and Ecuador 4, Chile and Venezuela 3, Costa Rica 2 and Perú, Nicaragua and Bolivia 1.
Figure 1. Latin American countries studying aquatic ecosystems. Brazil is the leading country with 31 publications, followed by México 10, Argentina, 7 Colombia 5, Cuba and Ecuador 4, Chile and Venezuela 3, Costa Rica 2 and Perú, Nicaragua and Bolivia 1.
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Water 13 02693 g002 550
Figure 2. Most common water sources studied in Latin American countries. Multiple water sources included: river and drinking water, recreational, and irrigation water. Other water sources included estuarine, thermal, groundwater and different recreational waters.
Figure 2. Most common water sources studied in Latin American countries. Multiple water sources included: river and drinking water, recreational, and irrigation water. Other water sources included estuarine, thermal, groundwater and different recreational waters.
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Water 13 02693 g003 550
Figure 3. Anthropogenic activities affecting water bodies. (A) Number of articles published on water use. (B) Percent of publications by region. Region 1: North America, Central America and the Caribbean (NCC); Region 2: South America (SA).
Figure 3. Anthropogenic activities affecting water bodies. (A) Number of articles published on water use. (B) Percent of publications by region. Region 1: North America, Central America and the Caribbean (NCC); Region 2: South America (SA).
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Table
Table 1. Percentage of studies that reported antimicrobial resistance in aquatic environments, by region and antibiotic class.
Table 1. Percentage of studies that reported antimicrobial resistance in aquatic environments, by region and antibiotic class.
Antibiotic GroupNCCSA
Aminoglucoside9389
Aminocumarine100NT
Amphenichol9283
AnsamycinNT100
Carbapenem4084
Carboxipenicillin100100
Cephalosporin (1st generation)100100
Cephalosporin (2nd generation)10090
Cephalosporin (3rd generation) 7996
Cephalosporin (4th generation)NT100
Fluoroquinolone10083
Glycopeptide10071
GlycylcyclineNT75
Inhibition nucleic acid synthesis10087
LincomycinNT100
Macrolide100100
Nitrofurane100100
Penicillin10094
Penicillin + betalactamase inhibitor8090
PhosphonicNT100
PolymyxinNT75
Quinolone87.583
Tetracycline10097
NT: non-tested.
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Domínguez, D.C.; Chacón, L.M.; Wallace, D. Anthropogenic Activities and the Problem of Antibiotic Resistance in Latin America: A Water Issue. Water 2021, 13, 2693. https://doi.org/10.3390/w13192693

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Domínguez DC, Chacón LM, Wallace D. Anthropogenic Activities and the Problem of Antibiotic Resistance in Latin America: A Water Issue. Water. 2021; 13(19):2693. https://doi.org/10.3390/w13192693

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Domínguez, Delfina C., Luz María Chacón, and D’Janique Wallace. 2021. "Anthropogenic Activities and the Problem of Antibiotic Resistance in Latin America: A Water Issue" Water 13, no. 19: 2693. https://doi.org/10.3390/w13192693

APA Style

Domínguez, D. C., Chacón, L. M., & Wallace, D. (2021). Anthropogenic Activities and the Problem of Antibiotic Resistance in Latin America: A Water Issue. Water, 13(19), 2693. https://doi.org/10.3390/w13192693

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