Review
A review of emerging organic contaminants (EOCs), antibiotic resistant bacteria (ARB), and antibiotic resistance genes (ARGs) in the environment: Increasing removal with wetlands and reducing environmental impacts

https://doi.org/10.1016/j.biortech.2020.123228Get rights and content

Highlights

Abstract

Emerging organic contaminants (EOCs) include a diverse group of chemical compounds, such as pharmaceuticals and personal care products (PPCPs), pesticides, hormones, surfactants, flame retardants and plasticizers. Many of these compounds are not significantly removed in conventional wastewater treatment plants and are discharged to the environment, presenting an increasing threat to both humans and natural ecosystems. Recently, antibiotics have received considerable attention due to growing microbial antibiotic-resistance in the environment. Constructed wetlands (CWs) have proven effective in removing many EOCs, including different antibiotics, before discharge of treated wastewater into the environment. Wastewater treatment systems that couple conventional treatment plants with constructed and natural wetlands offer a strategy to remove EOCs and reduce antibiotic resistant bacteria (ARB) and antibiotic resistance genes (ARGs) far more efficiently than conventional treatment alone. This review presents as overview of the current knowledge on the efficiency of different wetland systems in reducing EOCs and antibiotic resistance.

Introduction

In recent years there has been growing concern about the release of organic compounds of anthropogenic origin, known as emerging organic contaminants (EOCs), to the environment. These EOCs include a diverse group of thousands of chemical compounds, such as pharmaceuticals and personal care products (PPCPs), pesticides, hormones, surfactants, flame retardants, plasticizers and industrial additives, among others. Metabolites and intermediate degradation products of parent compounds are also included (Farré et al., 2008). The ubiquity of EOCs in the environment poses a threat to many non-target living organisms since they are designed to remain biologically active for long periods. The presence of antibiotics is of special concern due to the development of antibiotic resistant bacteria (ARB) and antibiotic resistance genes (ARGs). These substances are extensively used in both human and veterinary medicine against microbial infections and are excreted from the body of the treated organisms, together with their metabolties, within a few days of consumption. It has been widely demonstrated that conventional sewage treatment plants (STPs) are inefficient in the removal of many PPCPs, including antibiotics, ARBs and ARGs, thus contaminanting the receiving ecosystems with a complex mixture of bioactive agents and bacteria (Cacace et al., 2019, Corno et al., 2019, Manaia et al., 2018).

Once in the environment, antibiotics can lead to the continuous selection for ARB that contain ARGs (Choo, 1994, Costanzo et al., 2005, White et al., 2006: Ávila and García, 2015, Sui et al., 2015, Shiffett and Schubauer-Berigan, 2019). Although ARB are a threat to public health, ARGs are the underlying mechanism of an increasing antibiotic tolerant microbial consortia. In recent years, medical professionals and scientists globally have become concerned over the prevalence of ARGs and ARB that have appeared as the result of over prescription/production of antibiotics. Overuse of antibiotics can range from doctors prescribing them ineffectively to patients for viral infections (Gonzales et al., 1997), patients using other people’s antibiotics or old antibiotics and the use of antibiotics as growth promotors and feed additives in livestock and poultry (Kim and Aga, 2007). In 2019, antibiotic-resistant bacteria and fungus caused more than 2.8 million infections and 35,000 deaths in the United States alone (CDC, 2019). Currently, there are approximately 260 different antibiotics in about 20 different families or classes (Everage et al., 2014). A focus of this paper is to review how constructed and natural weltands can enhance removal of antibiotics.

In this paper, we review the occurrence and impact of EOCs, especially PPCPs, ARB and ARGs in the environment and address the potential of wetlands to remove these compounds from wastewaters. For PPCPs, we focus on antibiotics which are the main cause of ARB and ARGs. There are already several reviews on the occurrence of PPCPs in the environment and removal by constructed wetlands (García et al., 2010; Zhang et al., 2014), but few specifically focused on ARB and ARGs (Liu et al., 2019). The main objective of this paper is to discuss the prevalence of PPCPs, ARB, and ARGs in aquatic ecosystems and the mechanisms of removal using constructed and natural wetlands.

Section snippets

Sources of PPCPs, antibiotic resistant bacteria (ARB) and antibiotic resistance genes (ARGs)

After intake, antibiotics rarely become fully metabolized in the body and thus are partially excreted in their original form (Zhang et al., 2009). Together with their metabolites, they are excreted from the body through urine and feces within a few days of consumption. In rural areas, direct excretion from medicated cattle in animal husbandry facilities is the main entrance route into the environment, together with manure application as fertilization amendments (considering also biosolids from

Antibiotic resistance acquisition

It is important to understand that antibiotic resistance can be present in all bacteria, not solely pathogenic bacteria (Hawkey, 1998). Bacteria often have two distinct types of resistance to antibiotics, intrinsic and acquired resistance. Intrinsic resistance is a naturally occurring trait in the organism, while acquired resistance is the evolution of sensitive bacteria to resistant bacteria (Hawkey, 1998). Organisms most often develop resistance to antibiotics because of spontaneous mutations

PPCPs, ARB and ARGs in the environment and their impacts

The continued use of antibiotics is likely to increase the frequency of antibiotic resistance in the environment (Gillings and Stokes, 2012). For instance, soil samples in the Netherlands were shown to contain up to 15 times more genes-encoding resistance in 2008 when compared to soil samples from 1970 (Knapp et al., 2010). Furthermore, antibiotics can survive for extended periods of time in the environment and free DNA carrying ARGs can last up to two years in the soil.

Urban wetlands may

Efficiency of conventional wastewater treatment on PPCPs, ARB and ARGs removal

Secondary municipal wastewater treatment using conventional activated sludge (CAS) does not substantially remove PPCPs and removal rates are highly compound specific (Conkle et al., 2008; Ávila and García, 2015, García et al., 2010; Zhang et al., 2014). Removal mechanisms during CAS treatment include microbial degradation and sorption to particulate matter (Conkle et al, 2010). However, sludge can retain significant concentrations of PPCPs that can be released back into the environment after

Removal of EOCs, ARB and ARGs in constructed wetlands

Constructed wetlands (CWs) for wastewater treatment are a state of the art technology with thousands of full-scale applications at a global scale. CWs are being increasingly used for decentralized wastewater treatment due to their simple design and because operation and maintenance costs are typically much lower than conventional systems. Wetlands do not require any chemical addition and their sludge production is negligible (Álvarez et al., 2017, Paing et al., 2015). Efficiency of CWs for the

PPCPs in small-scale domestic (septic) treatment systems

In many areas with a low-density population, such as suburban and semi-rural situations, sewage treatment for a significant proportion of the population is provided by small-scale (septic tanks) and package plant treatment systems. For example, over 85% of the population in some areas of the United States use septic systems (Godfrey et al., 2007) mainly because conventional centralized systems for such populations is very expensive (Matamoros et al., 2009). Coastal Louisiana is an example of an

Reduction of PPCPs, ARB and ARGs in natural wetlands

Natural wetlands can also reduce PPCPs, as well as ARB and ARGs, in treated sewage effluents. Direct discharge to natural wetlands after treatment in a centralized STP can often result in significant removal of these compounds in a relatively small area. Hayward et al. (2018) reported that ARGs generally decreased in tundra wetland ecosystems receiving domestic wastewater, and that removal rates were inversely correlated with HRT. In this study, short HRTs (2 days) produced the highest ARGs

Conclusions

The presence of antibiotics selectively favors ARB and ARGs, so their reduction in wetlands needs to be an area of focus. Research on disinfection methods and the behavior of EOCs, ARB, and ARGs should continue to inform adaptive management of treatment systems to reduce the impact on the receiving environment, ensuring safety for both humans and other organisms. Overall, a well-managed treatment system coupling municipal wastewater treatment systems to wetlands can result in significant

CRediT authorship contribution statement

Joan Garcia: Writing - original draft. María Jesús Garcia-Galan: Writing - original draft. John W. Day: Writing - original draft. Raj Boopathy: Conceptualization, Writing - review & editing. John R. White: Writing - original draft. Scott Wallace: Writing - original draft. Rachael G. Hunter: Writing - original draft.

References (104)

  • J.L. Conkle et al.

    Reduction of pharmaceutically active compounds by a lagoon wetland wastewater treatment system in Southeast Louisiana

    Chemosphere

    (2008)
  • G. Corno et al.

    Effluents of wastewater treatment plants promote the rapid stabilization of the antibiotic resistome in receiving freshwater bodies

    Water Res.

    (2019)
  • S.D. Costanzo et al.

    Ecosystem response to antibiotics entering the aquatic environment

    Mar. Pollut. Bull.

    (2005)
  • O. Decamp et al.

    Abundance, biomass and viability of bacteria in wastewaters: impact of treatment in horizontal subsurface flow constructed wetlands

    Water Res.

    (2001)
  • S. Dires et al.

    Antibiotic resistant bacteria removal of subsurface flow constructed wetlands from hospital wastewater

    J. Environ. Chem. Eng.

    (2018)
  • Z. Dong et al.

    A potential new process for improving nitrogen removal in constructed wetlands-promoting coexistence of partial-nitrification and ANAMMOX

    Ecol. Eng.

    (2007)
  • T.J. Everage et al.

    A survey of antibiotic resistant bacteria in a sewage treatment plant in Thibodaux, Louisiana, USA

    Int. Biodeterior. Biodegrad.

    (2014)
  • H. Fang et al.

    Occurrence and elimination of antibiotic resistance genes in a long-term operation integrated surface flow constructed wetland

    Chemosphere

    (2017)
  • M. Farré et al.

    Fate and toxicity of emerging pollutants, their metabolites and transformation products in the aquatic environment

    Trends Anal. Chem.

    (2008)
  • J. García et al.

    Role of hydraulic retention time and granular medium in microbial removal in tertiary treatment reed beds

    Water Res.

    (2003)
  • M.R. Gillings et al.

    Are humans increasing bacterial evolvability?

    Trends Ecol. Evol.

    (2012)
  • R. Grabert et al.

    Effect of tetracycline on ammonia and carbon removal by the facultative bacteria in the anaerobic digester of a sewage treatment plant

    Bioresour. Technol.

    (2018)
  • M. Gros et al.

    Removal of pharmaceuticals during wastewater treatment and environmental risk assessment using hazard indexes

    Environ. Int.

    (2010)
  • J.L. Hayward et al.

    Fate of antibiotic resistance genes in two Arctic tundra wetlands impacted by municipal wastewater

    Sci. Total Environ.

    (2018)
  • Y. He et al.

    Evaluation of attenuation of pharmaceuticals, toxic potency, and antibiotic resistance genes in constructed wetlands treating wastewater effluents

    Sci. Total Environ.

    (2018)
  • C.D. Helt et al.

    Antibiotic resistance profiles of representative wetland bacteria and faecal indicators following ciprofloxacin exposure in lab-scale constructed mesocosms

    Ecol. Eng.

    (2012)
  • M. Hijosa-Valsero et al.

    Removal of antibiotics from urban wastewater by constructed wetland optimization

    Chemosphere

    (2011)
  • D. Hocquet et al.

    What happens in hospitals does not stay in hospitals: antibiotic-resistant bacteria in hospital wastewater systems

    J. Hosp. Infect.

    (2016)
  • X. Huang et al.

    Performance of vertical up-flow constructed wetlands on swine wastewater containing tetracyclines and tet genes

    Water Res.

    (2015)
  • X. Huang et al.

    Removal of antibiotics and resistance genes from swine wastewater using vertical flow constructed wetlands: Effect of hydraulic flow direction and substrate type

    Chem. Eng. J.

    (2017)
  • A. Jia et al.

    Occurrence and fate of quinolone and fluoroquinolone antibiotics in a municipal sewage treatment plant

    Water Res.

    (2012)
  • S. Kahl et al.

    Effect of design and operational conditions on the performance of subsurface flow treatment wetlands: Emerging organic contaminants as indicators

    Water Res.

    (2017)
  • B. Kasprzyk-Hordern et al.

    The removal of pharmaceuticals, personal care products, endocrine disruptors and illicit drugs during wastewater treatment and its impact on the quality of receiving waters

    Water Res.

    (2009)
  • E. Kassotaki et al.

    Enhanced sulfamethoxazole degradation through ammonia oxidizing bacteria co-metabolism and fate of transformation products

    Water Res.

    (2016)
  • Y. Li et al.

    A review on removing pharmaceutical contaminants from wastewater by constructed wetlands: design, performance and mechanism

    Sci. Total Environ.

    (2014)
  • L. Liu et al.

    Elimination of veterinary antibiotics and antibiotic resistance genes from swine wastewater in the vertical flow constructed wetlands

    Chemosphere

    (2013)
  • X. Liu et al.

    A review on removing antibiotics and antibiotic resistance genes from wastewater by constructed wetlands: Performance and microbial response

    Environ. Pollut.

    (2019)
  • X. Liu et al.

    Antibiotics in the aquatic environments: a review of lakes, China

    Sci. Total Environ.

    (2018)
  • R. Maal-Bared et al.

    Phenotypic antibiotic resistance of Escherichia coli and E. coli O157 isolated from water, sediment and biofilms in an agricultural watershed in British Columbia

    Sci. Total Environ.

    (2013)
  • J. Mamo et al.

    Fate of pharmaceuticals and their transformation products in integrated membrane systems for wastewater reclamation

    Chem. Eng. J.

    (2018)
  • C.M. Manaia et al.

    Antibiotic resistance in wastewater treatment plants: tackling the black box

    Environ. Int.

    (2018)
  • V. Matamoros et al.

    Preliminary screening of small-scale domestic wastewater treatment systems for removal of pharmaceutical and personal care products

    Water Res.

    (2009)
  • I. Michael et al.

    Urban wastewater treatment plants as hotspots for the release of antibiotics in the environment: a review

    Water Res.

    (2013)
  • A. Naquin et al.

    Presence of antibiotic resistance genes in a sewage treatment plant in Thibodaux, Louisiana, USA

    Bioresour. Technol.

    (2015)
  • J. Nivala et al.

    Dynamics of emerging organic contaminant removal in conventional and intensified subsurface flow treatment wetlands

    Sci. Total Environ.

    (2019)
  • H. Nõlvak et al.

    Dynamics of antibiotic resistance genes and their relationships with system treatment efficiency in a horizontal subsurface flow constructed wetland

    Sci. Total Environ.

    (2013)
  • J. Paing et al.

    Effect of climate, wastewater composition, loading rates, system age and design on performances of French vertical flow constructed wetlands: a survey based on 169 full scale systems

    Ecol. Eng.

    (2015)
  • C. Pelissari et al.

    Nitrogen transforming bacteria within a full-scale partially saturated vertical subsurface flow constructed wetland treating urban wastewater

    Sci. Total Environ.

    (2017)
  • C. Pelissari et al.

    Effects of partially saturated conditions on the metabolically active microbiome and on nitrogen removal in vertical subsurface flow constructed wetlands

    Water Res.

    (2018)
  • P.J. Phillips et al.

    Concentrations of hormones, pharmaceuticals and other micropollutants in groundwater affected by septic systems in New England and New York

    Sci. Total Environ.

    (2015)
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