This review describes a new means of control and stimulation of microorganisms involved in the bioremediation of sediments and waterlogged soils. This emerging technology is derived from sedimentary microbial fuel cells, and consists in ensuring aerobic respiration of aerobic microbial populations in anaerobic conditions by means of a fixed potential anode in order to evacuate the electrons coming from the microbial respiratory chains. This review describes the conceptual basis of the electro-bioremediation, the material devices used (electrode set-ups and spacing), and finally studies the various devices published since the bench tests until the scarce in-field implementations.
The world’s population grows and concentrates in urban areas [
In latest decade, the electro-bioremediation has attracted growing attention, but to date no review has focused on means to direct it, to limit its GHG emissions [
According to European Environmental Agency, self-purification is the ability for any water body to removal the organic material, mineral nutrients, or other pollutants by the natural activity of its resident biological communities. It is a natural biogeochemical processes leading to the oxidation and mineralization of organic matter, and it is particularly active in the river underflow (hyporheic zone) where a redox gradient naturally installs [
Sediment is generally oxygen poor (consumed by microorganisms) and OM laden, so microbial metabolism maintains reducing conditions in sediment where the biodegradation reactions take place according to a redox gradient (
In running waters, bio-geo-electrochemical processes are not so gradually organized as described in lake sediments according to depth [
Water system metabolic activity transforms a huge fraction of OM [
corresponds to 25 kg of CO2 over a 100 year period [
The ultimate step of OM degradation in anoxic condition is methanogenesis. CH4 is predominantly produced from either acetate (acetoclastic methanogenesis) or hydrogen and carbon dioxide (hydrogenoclastic methanogenesis) [
According to the United States EPA, Bioremediation is “an engineered technology that modifies environmental conditions to encourage microorganisms to destroy or detoxify organic and inorganic contaminants in the environment”. Technologies can be generally classified as in-situ bioremediation treating the contaminated medium on the site or ex-situ bioremediation involving the contaminated medium extraction to treat it elsewhere [
Over the past decade, a new biological discipline, the electro-microbiology, was a rapidly emerging field from the microbiology. It deals with the interactions between microorganisms and electronic devices, and novel electrical properties of microorganisms [
Bacteria can direct transfer their electrons to solid surfaces acting as anode by different electron-transferring mechanisms summarized in
1) Indirect electron transfer by externally added mediators (methyl-viologen aka Paraquat; potassium ferricyanide; methylene blue or natural mediators (humic substances, Fe(II)/Fe(III), or SO 4 2 − /H2S [
2) Indirect electron transfer by self-produced mediators (electron shuttles) released by microorganisms (e.g. flavins of Shewanella sp. or piocyanin of Pseudomonas sp.), the oxidized mediator is reduced on the outer cell membrane, and then the reduced mediator transfer it electron to anode. This transfer mechanism depends on diffusive fluxes inside the biofilm;
3) Short-range direct electron transfer by outer membrane-bound redox systems, such as c-type cytochromes, to anode (Clostridium sp.; Desulfotomaculum sp.; Shewanella sp.; Aeromonas sp.) [
4) Long-range direct electron transfer through the biofilm via electrically conductive “nanowires” (pili), Geobacter sp.; Desulfuromonas sp.) [
A smart solution is to supply electron acceptors via direct electrochemical means, forming a Microbial-Electrochemical System (or Bio-Electrochemical Systems aka BESs). It harnesses the microbial ability to direct or indirect transfer electrons to solid surfaces by using a conductive electrode acting acts as either an electron acceptor or donor depending on the polarity conditions.
Microbial Fuel Cell is a BES which generates electricity, and Microbial Electrolysis Cell (MEC) is a BES requiring a power supply to drive non-spontaneous reactions. Many of the recent advances in the electron transfer between microbes and electrodes have arisen from the study of MFCs, devices initially designed for harvesting electricity from OM degradation [
Initially designed to run with marine sediment rich in organic matter and sulfides [
BMFC can be used to explore some new bioremediation ways, which neither seek the maximum electron mining, nor inject energy to catalyse high added value products. The electron flux is managed to maintain an anode microbial population conducive to the MO biodegradation, and avoiding the production of undesirable gases (N2O, CH4 & H2S). The surplus collected electrons will go power the potentiostat, the sensing and control device, in charge to keep a proper voltage. The BMFC principle applied to constructed wetlands leads to the emergence of new environmental engineering, see below §5.2.
Bioremediation aims at increasing the OM assimilation while overcoming the microbial metabolism limits due to a shortage of electron acceptors. A basic approach is to provide chemical compounds as electron acceptors (i.e., oxidation) to increase OM degradation or electron donors (i.e. reduction) to increase the refractory OM degradation (e.g. organo-halogenated pollutants) and the electrochemical bioremediation (
Generally, OM is the electron donor in bioremediation processes in polluted environments. Acceleration of self-purification based on metabolic activities of
natural sedimentary microorganisms is a widely accepted durable solution in environmental engineering, but its relatively low efficiency and delicate control considerably limit its actual application. A faster electron transfer to more conductive anode is assumed lead to sizable increase in OM oxidation rate, compared with natural electron acceptors [
Even if the redox potentials shown in
As the natural redox potential difference between oxygenated superficial water and anoxic sediments is generally ≈800 mV, between 770 and 870 mV [
The electro-bioremediation development is not only possible but desirable for its advantages. Firstly, it stimulates the contaminant removal without require neither chemical addition nor energy input, so the operational cost can be significantly lower than other remedial methods; moreover, it produces electrical current, which can power a remote monitoring device, and finally it is presumed lead to higher treatment efficiencies than with conventional biological processes [
The construction and analysis of BMFCs requires thorough knowledge in separate scientific and engineering fields, ranging from microbiology and electrochemistry to materials and environmental engineering [
In BMFC the anode is in charge of collect the microbial respiration electrons; therefore, anodic materials must be conductive, chemically stable and non-ha- zardous in environmental conditions, and high degree of biocompatibility to all avoid any toxic effect upon the microorganisms. In BMFC the cathode is in charge to waste the anode electrons by reducing oxidized compounds. Oxygen is the most suitable electron acceptor because of its high oxidation potential, availability, low cost, sustainability, and the lack of any chemical waste production (water is the sole waste). The cathode must obviously have the same properties as the anode, but furthermore, the need to float on the water surface in order to maximum benefit of the oxygen concentration in air, imposes light and porous cathode materials, to facilitate oxygen access. So, soft carbon-based materials (felt, fabrics) stretched over resistant stainless steel frame or supported by polystyrene floats [
Obviously electrodes made of Cu must be prohibited, due to the high toxicity of Cu2+ to microorganisms, but some noncorrosive metal electrode as stainless steel mesh or titanium can be utilized [
Carbon-based electrodes are the most widely used in MFCs studies. Except non electrical conductive diamond (sp3 carbon), all the allotropic forms of carbon (amorphous carbon, glassy carbon, graphite, graphene and nanotubes) are used with various designs as electrode materials. Graphite plate anodes have been commonly adopted in early BMFC designs but they are difficult and costly to bury into the sediment. Graphite rod is more easily inserted than plate, but it presents relatively low surface area. Carbone felts offer a large colonization surface to bacteria, but are more difficult to install in sediments. Hence, selection of electrode material and design of its structure need special attention. In a synthetic review, Guo et al. (2015) examine impact on microorganism-electrode exchanges and electron transfer mechanisms of electrode surface topography and chemistry, and propose three relevant impact class at different scales [
1) Adherence of the cells;
2) Formation and structure of the electroactive biofilm;
3) Electrical connectivity between the cells and the electrode in a direct or indirect ways.
Because of its excellent electrical conductivity and chemical stability, the graphite (graphite rod, plate or sheet and graphite fibre brush) is one of the most commonly used electrode materials [
In terms of configuration, Wei et al. (2011) divided carbon-based electrodes into plane, packed, and brush structures [
3D structures are of particular benefit because they provide large available surface areas for bacterial colonization and substrate transport, solid and macroporous structures for redox reactions, electron transfers. One way to increase the surface area free to bacteria is the use of loose granular materials, such as granular graphite, or activated carbon, is one possible way. GAC electrode can be designed as a diffuse electrode, distributed into the sediment in order to develop a maximum contact surface with the sediment bacteria. Packed into a polypropylene mesh bag, GAC is inserted into sediment [
Activated carbon felts have exceptional properties as a high electronic conductivity, low weight, good chemical stability, and low cost. However, the study of their intrinsic properties is a bit difficult due to their hydrophobicity and compressibility [
- high porosity (99% if uncompressed material);
- great compressibility which makes it difficult to reproduce a constant electrode quality upon replacement in device;
- Variable electrical conduction through carbon/carbon or graphite/graphite contacts, depending on the contact strength. Indeed, felts are made of short fibres, ≈10 mm Æ, and giving an exceedingly large number of contacts fibre to fibre. Also, the overall electrical conduction pattern is complex, depending on the degree of compression.
More elaborated nano-structures can be used, as carbon multiwalled nanotubes or carbon nanopowder immobilized in conductive adhesive on electrode surface [
Electrode surface chemistry impacts the microbe-electrode interactions by many ways: 1) surface charge attraction; 2) hydrogen bonding; 3) van der Waals force; 4) immobilized mediator; 5) random roughness; 6) oriented nano-pattern and nanoparticles; and 7) hydrophilic properties of electrode surface, fostering a fast bacterial adhesion onto the electrode surface. Electrochemically active microorganisms attach preferentially on hydrophilic and positively charged surfaces [
or activated carbon) on stainless steel fibre felts gives an open, solid and macro-porous structure, providing large surface area electrodes for reaction, interfacial transport and biocompatible interface available for bacterial colonization and substrate transport. Graphene modified anode delivered a maximum power density of 2142 mW/m2 at a current density of 6.1 A/m2, greatly improved compared with the unmodified stainless steel fibre felts [
A huge fraction of the ohmic loss in BMFC is caused by the electrode spacing. Unlike laboratory cells where chambers are only separate by thin membrane and electrode spacing can be easily reduced, in BMFC, limits exist due to the natural spatial separation existing between sediment oxic and anoxic zones. The best depth to embed anode in sediment should relatively shallow, between 3 cm [
Tubular-type BES is constructed by winding together the anode, separator, and cathode layers around a perforated PVC tube, with the cathode facing inside and exposed to air, and the anode exposed to the surrounding matrix [
U-tube BMFC consists in an air-cathode placed inside the anode chamber and had been proven to be efficient for electricity recovery due to the low internal resistance [
Snorkel BMFC consists in a single conductive tube (snorkel) properly set to create an electrochemical linking between the anoxic zone (polluted sediment) and the oxic zone (superficial oxygenated water). The lower part is buried within sediment and plays the role of anode, accepting electrons from the organic matter oxidation. Electrons flow along the snorkel up to the part exposed to the aerobic environment (cathode part), where they reduce oxygen to form water [
Another major concern in electro-bioremediation field-scale application is the low ratio between the limited volume under anode influence and the large sediment volumes to be treated. Indeed, with a conventional BMFC, the affected sediment radius by anode is very narrow, typically about few centimetres around the anode [
BMFC scaling-up do not consist in its size rising, as any increasing of electrode surface area results in decreased power density. As alternative to the physical scale-up of BMFCs, it is possible to scale up power by using smaller-sized BMFCs operating alone connected to a power management system and managed them in such way to maintain a sufficiently low redox potential for a total denitrification up to N2, and/or a full anammox, resulting in no accumulation of N2O, but without reaching the potential formation of H2S and CH4.
Classical electrical circuit includes voltage meters (or a potentiostat to a finer understanding of the system) connected in parallel to properly measure cell voltages and potentials between electrodes. The current is calculated as a function of the voltage (U, Volt) and the external resistance (R, Ohm) according to Ohm's law, I = U/R. A potentiostat can also operate in a two-electrode setup to obtain polarization curves or to determine the ohmic resistance of the MFC with the current interrupt method. The power output (P, Watt) is calculated according to P = UI. The potentials of anode and cathode electrodes were measured according to a reference electrode of Ag/AgCl in a three electrode setup [
CH4 production and anode potential are linked, suggesting the anode potential influences the competition between anode respiring bacteria and methanogens for substrates [
1) Starting from the open circuit voltage at zero current, there is an initial steep voltage decrease: the activation losses dominate and redox reaction kinetics is limiting. Anode respiring bacteria can lower this overpotential by optimizing their electron-transfer strategies and thus increase their own metabolic activity. These interactions between biomass and anode are related to the anode surface properties;
2) Then the voltage falls more slowly, fairly linear with current: the ohmic losses dominate, due to ion transfer. Porewater H+ and cations flowing toward the cathode, faces a resistance adding ohmic losses in sediment. Additionally, the anode resistance (materials and connexions) introduces an ohmic voltage loss and hampers the electron flux. The highest currents ensure the highest rate for OM oxidation. But generally in-field BMFC suffers from high over-potential, especially in freshwater milieu where porewater conductivity is low;
3) Finally, at higher currents the voltage rapid falls: there the mass transfer losses dominate, due the reactions at the electrodes are limited by the ability of the reactants and products to move toward and away from the electrode. For a maximum self-purification, the substrate supply in sediment should be at least equivalent to the electron extraction capacity of the anode. The anode design is an important factor to avoid any anode saturation. The H+ diffusion resistance through sediment and biofilms results in local pH increase which may adversely affect bacterial physiology and thus self-purification processes. Another possible way to reduce the mass transfer losses is to increase the anode contact areas with the sediment. But this raises the ohmic losses due to increased current flow and to a dissimilar distribution of potentials. These problems are less important at the cathode as with floating cathode, rapidly colonized by bacteria, and where oxygen concentration is saturating [
Theoretically, a BMFC can directly feed its power management system (PMS), but two main obstacles must be overcome: 1) the production of a low potential of max 0.8 V, unusable as-is by most electronic devices requiring at last 0.9 V to 1.8 V; and 2) the power production intermittence. Both particularities request a PMS able to stock and concentrate the harvested energy. To meet these requirements capacitors have been used to store harvested energy and then deliver it in short bursts of high-power to power sensors [
There are three test levels in electro-bioremediation studies: 1) bench tests in microbial fuel cells (<1 L volume); 2) pilot tests on well-equipped semi-industrial devices (>1 L volume) are usually small-scale field-tests and are essential before site implementation to optimize redox processes in BMFC. They constitute the majority of work on the setup merging constructed wetlands and MFC; and 3) field tests with quasi-industrial-scale projects. According to our classification the two first levels deal with SMFCs, and only the field studies concerns the BMFCs themselves. The voltage stabilization time can vary, depending largely on the size and complexity of the device. In bench tests the voltage stabilizes after about ten days: 2 - 3 days for marine sediment [
Allowing easier manipulations and testing, bench tests are performed on sediment samples from the natural site and studied into two-chamber cell, or vials for laboratory-scale runs. This study scale is often referred to as a microcosm study and focuses on the electro-biodegradation of contaminants such as pesticides [
Pesticides and oil products are among the most common and harmful subsurface contaminants due to their extensive use, persistence in the environment, and toxicity. The microbiological processes, involved in bio-electrochemical remediation of recalcitrant pollutants, are currently not fully understood, particularly in relation to electron transfer mechanisms. Some reviews provide a comprehensive analysis of the research on bio-electrochemical remediation and of the key parameters involved in the process [
Lab-scale study of a diesel-fed MFC shows clear effects of the prior electrode enrichment on diesel removing from polluted groundwater (complete removal of diesel 800 mg/L within 30 days) and current generation, going from 15.04 mW/m2 (without prior inoculation), to 90.81 mW/m2. Therefore, a prerequisite step in electro-bioremediation should be a selective enrichment of the anodic electrode (bio-augmentation) to enhance its degradation capability [
Inoculum | MFC | Medium | Removal yield | Anode material | Regulation | Potential | Ref. |
---|---|---|---|---|---|---|---|
Natural microbial consortium | 100 mL Single cell | contaminated marine sediment | 24% removal/66 d from 16 g/kg total petroleum hydrocarbons | carbon cloth | 1000 Ω resistor | n.d. | [ |
Natural microbial consortium | Snorkel in 120 mL serum bottles | artificially contaminated marine sediment (crude oil) | Up to 22% removal/200d | Graphite rods | n.a. | n.a. | [ |
Pure culture of Geobacter metallireducens and G. sulfurreducens | 250 mL dual-chamber | River sediment | reduce nitrate to nitrite | graphite | Potentiostat poised | −500 mV | [ |
Pure culture of G. metallireducens | 250 mL dual-chamber | hydrocarbon-contaminated harbour sediment | [14C]-toluene (≈90% removal/7 d) and [14C]-benzene (≈35% removal/9 d) | solid graphite stick | Potentiostat poised | + 300 mV (vs Ag/AgCL) | [ |
Pure culture of G. lovleyi | 250 mL dual-chamber | Synthetic growth medium | Tetrachloroethene removal rate: 25 µmol/d | graphite lectrode | Potentiostat poised | +500 mV or −300 mV (NHE) | [ |
Mixed culture dominated by sulphate reducers | 250 mL dual-chamber | artificial sea water + hydrocarbon-contaminated marine sediment | Toluene removal rate: ≈1 mg/(L.d) | Graphite plate | Potentiostat poised | +300mV (Ag/AgCl) | [ |
Mixed culture rich in γ-Proteobacteria, in mineral medium | 320 mL single cell | Anode biofilms in artificial medium | 93.5 removal from 8000 mg/L within 30 d | Carbon fibre brush | external resistance of 1000 Ω | n.a. | [ |
Natural microbial consortium | Snorkel, PVC 10 cm column, granular coal filled, stainless steel mesh stopper (400 × 400 mm) in sediment tank | Swamp sediment | 8% - 18% organic matter removal/120 d | stainless steel mesh | No poised | 200 mV | [ |
Natural microbial consortium | 2.5 L, 1.2 m cylinder in PVC, Ø 5 cm | 100 cm organic-rich sediment; and overlying water from pond | stainless steel bottle brush | 1000 Ω resistor | [ | ||
Natural microbial consortium | 3 L, Tubular MFC PVC tube (20 cm, Ø 3.5 cm) | Waterlogged diesel and engine oil contaminated soil | 63.5% - 78.7% removal/64 d (37.6% - 43.4% in open control) | carbon cloth or biochar | 100 Ω resistor | [ | |
Natural microbial consortium | 4 L Plexiglas column (35 cm, Ø 12 cm) | 0 - 10 cm depth lake sediment | 92% benzo[a]pyrene removal/970d (54% in controls) | graphite felt | 100 Ω resistor | 132 ± 24 mV (NHE) | [ |
Concentrated anaerobic sludge from WWTP | 35 L, 50 cm cylinder in polyacrylate, Ø 30 cm | Artificial constructed wetland soil, Ipomoea aquatica planted | 61% brilliant red X-3B dye decolorisation/3d hydraulic retention time | Granular activated carbone | 1000 Ω resistor | [ | |
Natural microbial consortium | Water tank: 390 L, L:120 cm, l: 50 cm, h: 65 cm | River sediment | 74% PAH removal/72 d | Carbon mesh on porous honeycomb- structure | 10 Ω resistor | 150 mV (Ag/AgCl) | [ |
of organochlorine compounds as tetrachloroethene to cis-dichloroethene [
The pilot tests aim at build more realistic field conditions than the bench tests. Microbial metabolism and community structure distinctively respond to the electro-bioremediation [
The merging of two nature-based technologies (constructed wetlands (CWs) and MFCs), is especially relevant since both are based on the microbial action to degrade wastewater contaminants. CWs are engineered water bodies planted with aquatic vegetation (macrophytes) designed to treating municipal or industrial wastewater or storm water runoffs. The biofilms associated to plant roots or to the bed filter material, are supposed to be the responsible for the degradation efficiency of CWs [
- Incorporating selected plants could prevent CH4 and N2O production by the system [
- Smart hydraulic management can limit the GHG production in CWs. Management of hydraulic retention time, intermittent loading and pulsing hydrologic regimes have also been recommended [
A paddy field is a flooded parcel of arable land used for growing rice and other semiaquatic crops. As their CH4 emissions likely contribute about 9% of total global anthropogenic emissions [
To our knowledge there is no effective full-scale implementation of electro-bio- remediation on the field [
The first field setup designed to energy productions consist in two graphite or stainless steel electrodes positioned parallel ≈20 - 40 cm above and below the sediment-water interface is set up in marine environment [
In principle, the use of electrodes to stimulate the microbiological oxidation of OM in water bodies is extremely appealing since they can potentially serve as permanent, low-cost and low maintenance electron acceptor. But BMFCs need significant improvements to become effective and controlled environmental remediation systems, widely accepted. The achievement of efficient, reliable and robust in-field electro-bioremediation, demands a setup tailored to the specific conditions of each site. And finally, resistance of operational bioremediation devices to the harsh outside conditions must be early integrated, at design stage, taking into account the specific conditions at the installation site.
Potential management needs more studies and optimisation efforts the in order to finer control bioremediation processes. Sadly almost all the articles dealing with the electrical management optimization of the MFCs concern the energy production. The resistance of the external circuit in an MFC directly influences the anode potential and the resultant bioavailability of the anode for anode respiring bacteria, giving the proper parameter to influence anode biofilm development and performance [
The ecological impacts of electro-bioremediation in real-world should be stressed and taken into account in the overall system engineering. Indeed, environmental conditions are known to deeply affect microbial communities in constructed wetlands, and therefore carbon, nitrogen and sulphur cycles [
Finally, to foster a widespread acceptance and practical setups of this new technology, we have to paid equal attention its potential risks on the sur-round- ing ecological system and society. If subjects such as the fight against GHGs or the use of clean energies are widely accepted socially, others are touchier. Indeed, as is the case for some other new technologies, such as genetic modifications, different socio-psychological factors could potentially influence societal acceptance of in situ electro-bioremediation due to use of some “touchy issues” such as nanoparticles or toxic elements on electrodes. We must further consider how citizens make trade-offs between perceived risk and benefit, in particular in controversial application areas such as the nanotech and the so called nature invasive technologies.
More broadly to reduce maintenance costs, involvement and empowerment of local residents require a knowledge transfer in order to favor the appropriation of installed devices and ensure their sustainability over time. The new electro bioremediation solutions specifically in urban or peri-urban locations must be co-designed/developed and co-implemented in multi-stakeholder and participatory context. It is the only guarantee of the success of sustainable operation over time.
Electro-chemically enhanced self-purification is a new frontier needing an interdisciplinary research. It is regarded as a new sustainable and effective strategy for treatment of polluted environments, because it eliminates the injection of expensive chemicals and reduces operational energetic cost as compared to other technologies. From merging of concepts of bioremediation, electron extraction and SMFC, the idea emerges to fine tune electrochemically biodegradation processes to guide them to specific benign products. The possibility of a totally passive system, self-powered by the excess electron flux provided by microbial activity is particularly attractive. The envisioned device will impose a potential difference favouring denitrifying consortia, and banning to methanogens and sulphate-reducing bacteria, producing CH4 and H2S respectively. In this concept we do not inject any electrons, but we fine-tune the anode potential in order to just accept the right amount of electron needed to keep a selected microbial activity, we passively pumps the electrons from anode respiring bacteria, and thus, drive microbial respiratory metabolism. Snorkel technique potentially represents a ground-breaking alternative to more expensive remediation options, further research efforts are needed to clarify factors and conditions affecting the snorkel-driven biodegradation processes and to identify suitable configurations for field applications. Promising results have been obtained using electro-bioremediation technologies at pilot scales, showing that these technologies may be implemented in the near future at field scales. But the two major foreseeable obstacles to the scaling-up, from the pilot scale to in-field implementation, to overcome are:
1) Maximizing the contact between anode respiring bacteria and the anode, and thus enhance the mediated oxidation processes. This will require a working on the anode geometry and its structure but also on its in-site implementation;
2) Simplify and ruggedize the system of regulation of the potential, in order to have an actual field-system, energetically autonomous and low maintenance cost.
The design and operational conditions must also be optimized to reduce the device internal resistance and improve electrochemical processes. Finally the design and engineering on the site receiving the bioremediation device are yet to be imagined, and will obviously have to be tailored to the specificities of each implementation site (e.g. geomorphology, climate, flow regime, pollutant loads). In the future, more attention should be pay to electro-bioremediation technology scaling up and in particular investigate their economic feasibility and field problems arising from the scale-up.
The authors thank the French National Research Agency (ANR 14-OHRI-0016 El Hamico), the Field Observatory in Urban Water Management (OTHU― http://www.othu.org/, FED4161), the Rhône-Alpes Region ARC 3 Environment, ENVIMED 2015 El Encobio and Campus France (PHC Utique Carthago 17G1006 and Imhotep Mareotis 37585QA) for their scientific and financial support.
Jobin, L. and Namour, P. (2017) Bioremediation in Water Environment: Controlled Electro-Stimulation of Organic Matter Self-Purification in Aquatic Environments. Advances in Microbiology, 7, 813-852. https://doi.org/10.4236/aim.2017.712064