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A decade of progress and turning points in the understanding of bio-improved


soils: A review

Article · March 2019


DOI: 10.1016/j.gete.2019.03.001

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Contents lists available at ScienceDirect

Geomechanics for Energy and the Environment


journal homepage: www.elsevier.com/locate/gete

A decade of progress and turning points in the understanding of


bio-improved soils: A review
Dimitrios Terzis *, Lyesse Laloui
Swiss Federal Institute of Technology (EPFL), Lausanne, Switzerland

highlights

• Reference is made to over forty studies produced after 2016.


• A look back on how far research has gone and a look to opportunities and challenges.
• 6 sections cover turning points which improved the understanding of MICP.
• Bio-inspired technologies do push forward the limits of thinking.

article info a b s t r a c t
Article history: Research and practice in the broader fields of civil and geotechnical engineering had long ignored the
Received 30 July 2018 presence of living microorganisms in the subsurface and the way it impacts conventional practices.
Received in revised form 8 January 2019 In the last 10 years, the term ‘‘microbial induced calcite precipitation’’, or that of ‘‘biogrouting’’ have
Accepted 4 March 2019
gained momentum in the scientific literature. They are often presented as the ‘‘next big thing’’ in
Available online xxxx
geotechnical engineering applications that will solve many kinds of problems, ranging from soil erosion
to landslide risk mitigation and liquefaction protection. Are the claimed benefits of the application of
microorganisms in conventional geotechnical problems real? The present review work aims to shape
a complete and comprehensive understanding of the progress reported in the field of bio-mediated
soil improvement. Specific focus is put on pivotal points in this decade-long path which is marked by
proof of fundamental concepts at multiple scales. Among the treated literature, reference is made to
over forty studies produced after 2016. As soil bio-reinforcement makes its steps towards claiming a
spot in mainstream geotechnical practice this review foresees to offer both a look back on how far
research has gone and a look forward by evaluating opportunities and challenges which lie ahead.
© 2019 Published by Elsevier Ltd.

1. Engineering nature-based and nature-inspired solutions The major role of bacteria in applications has been addressed
in various fields ranging from agriculture, to enhance crop nu-
Water, a constituent element of life found below the earth’s trition, or protect crops against pathogens,2 to electricity or light
surface, attracted the interest of researchers and engineers, as production, wastewater treatment and environmental remedia-
early as the fundamental theories of modern geotechnical en- tion. Starting from the aquatic environment, specific bacterial
gineering were established. However, whilst eighty per cent of strains have been identified and attracted the interest of re-
Earth’s total dry biomass is found below its surface,1 the role searchers due to their ability to produce electricity. The first
of microorganisms in subterranean engineering applications re- relevant ideas appeared as early as 1911.3 Decades later, progress
mained, until recently, relatively underexplored. Before moving has been reported and a specific type of bacteria has been iden-
our focus to soil bio-improvement, it is pertinent to consider tified, such as strains of Shewanella Oneidensis, which are able
that some of these microorganisms carry the oldest and most to conduct electrical current by using metals as intakes.4,5 Re-
fascinating mechanisms and genetic sequences that nature had cent applications mobilize such strains as potential agents for
millions of years of evolution to bring to perfection. wastewater treatment6 and electricity production.7
However, many of the implemented technologies which mo-
bilize unicellular organisms often require genetic modifications
to be done. Limitations thus emerge as far as their exploitation
* Corresponding author.
E-mail address: dimitrios.terzis@epfl.ch (D. Terzis). is concerned since current regulations do not allow modified

https://doi.org/10.1016/j.gete.2019.03.001
2352-3808/© 2019 Published by Elsevier Ltd.

Please cite this article in press as: Terzis D. and Laloui L., A decade of progress and turning points in the understanding of bio-improved soils: A review, Geomechanics
for Energy and the Environment (2019), https://doi.org/10.1016/j.gete.2019.03.001.
2 D. Terzis and L. Laloui / Geomechanics for Energy and the Environment xxx (xxxx) xxx

organisms to be released into the environment. Their use re- of efficiency. Nature itself is the perfect example of achieving
mains within laboratories and their integration into real-world maximum performance at minimum energy needs. The authors
problems is doubtful. New types of technology emerge to over- believe that emerging technologies, which have at their core
come such limitations. This refers to technologies which do not biological processes, do push forward the limits of thinking which
require whole bacterial cells but only a specific protein or enzyme inevitably will lead to progress, regardless of the individual fate
found inside the cell walls, which can be isolated and extracted of each individual mechanism discussed above.
to execute genetic codes and reaction sequences. These latter
applications are often referred to as ‘‘cell-free’’8 technologies 2. Bio-mediated urea hydrolysis and CaCO3 mineralization
since they do not require whole cells but individual genetic
sequences and proteins found within the cell cluster or exerted The overview on the crossroads between biology and geo-
in its surrounding. engineering applications is herein narrowed down to the specific
Going beyond the direct use of microorganisms or their prod- case of bio-mineralization. Such mechanism is found in the core
ucts in engineering processes, we identify another trend at the of some of the aforementioned applications like those reported
crossroads of biomimicry and synthetic chemistry. Observations by Achal et al.,23 Jonkers et al.,16 Bernardi et al.24 and Stylo
of natural mechanisms have led to the development of new con- et al.14 It is pertinent to take into consideration the following
ceptual frameworks to address engineering problems such as, for clarification, regarding the use of the terms bio-mineralization
example, those referring to self-healing materials9,10 inspired by and bio-mediated mineralization. Bio-mineralization stands for
wound healing processes in plants and bones, or to development an organism’s capacity to produce and grow mineral structures
of performant fibre optics, based on spider silk.11 As another within its body as part of bones or tissues. The bio-mineralized
example, the unique architecture and properties of moth eye, element is composed mainly of calcium and phosphate with
which are responsible for eliminating light reflection, gave birth calcium carbonate commonly found in corals or shells of marine
to new concepts integrated in solar panel cells12 for achieving organisms. Bio-mediated mineralization characterizes nucleation
increased performance and efficiency in solar energy production. of particles which do not grow within the organism’s body, or on
Moving from the aquatic environment and the fields of ma- its tissues, but rather in the surrounding environment. The min-
terial sciences and biomimicry to the earth’s subsurface, one eralized elements are considered as a byproduct of the organism’s
can observe that during the past decade, innovative solutions biological processes, or are due to changes in surrounding envi-
that incorporate biological agents and mobilize natural pro- ronmental conditions, such as pH or concentration of chemical
cesses emerge. Amongst such novel approaches and applications species.
are those that reduce heavy metals and radioactive pollutants, Urea (CH4 N2 O) hydrolysis, or ureolysis, is such a chemical
such as uranium, from soils via bioremediation,13,14 produce reaction which generates favourable conditions which lead to
self-healing concrete15–17 for crack repair, and trace fractures in precipitation of solid mineral calcium carbonate. Ureolysis occurs
oil and gas reservoir formations with recent a field application in in natural environments without the presence of organisms or it
Switzerland.18 In the same context, knowledge has been evolving can be catalyzed as a result of the metabolic activity of species
in the past years around a technique applied to enhance oil due to the presence of the urease enzyme. CaCO3 nuclei are
extraction from trapped pores within reservoirs via the use of considered indirect products of urea hydrolysis, which precipitate
microbes. This technique is commonly referred to as Microbial in carbonate-rich solutions under increased pH and under the
Enhanced Oil Recovery (MEOR) and has shown signs of economic presence of a calcium source. More precisely, urea hydrolysis
efficiency for the secondary and tertiary phases of oil recovery refers to the decomposition of one mole of urea into two moles of
from reservoirs.19 ammonium and one mole of carbonate anion as shown in Eq. (1).
Bio-mediated and bio-inspired geo-mechanics opened new
horizons for innovative applications which provide unconven- CH4 N2 O + 2H2 O → 2NH4+ + CO23− (1)
tional solutions in geo-engineering problems.20 Some of these
Catalysis by the urease enzyme is found to lead to overall
applications remain in a rather hypothetical sphere, such as con-
faster completion times32 up to a factor of 1014 . The release of
ceptual designs of systems of foundations and anchors inspired
ammonium into the environment, due to urea hydrolysis, induces
from tree roots, or excavation systems inspired by the digging
pH increase, which is considered favourable for precipitation of
process observed in ant communities.21,22 Others target more
CaCO3 under the presence of carbonate ions and the introduction
practical applications such as the production of construction ele-
of a calcium source into the system (Eq. (2)).
ments out of earth materials. This is the case of bio-bricks, a term
used23,24 to describe bricks manufactured by mobilizing Micro- Ca2+ + CO23− → CaCO3 ↓ (2)
bial Induced Calcite Precipitation (MICP) in prefabricated moulds.
Such approaches for the manufacturing of construction elements This mechanism of calcium carbonate mineralization is consid-
out of geo-materials triggered the curiosity of researchers who ered of utmost ecological and geological importance. Biological
extend these concepts in the framework of future deep-space mechanisms which trigger and govern this process are associated
human missions where the inherent capacity of microorganisms with the reduction of carbon dioxide (CO2 ) in the atmosphere
to withstand extreme environmental conditions can be used for and its mineralization to calcium carbonate (CaCO3 ). Such is the
building purposes.25–27 case of cyanobacteria33 or plants which are found to capture CO2
Another example relates to the presence of gas bubbles or from the atmosphere and precipitate it around their roots into
the provision of gas bubble generation in saturated sand which CaCO3 crystals. Canavalia ensiformis (jack bean) for example is
is considered to substantially mitigate liquefaction risks.28,29 To considered such an ureolytic plant which has been studied for its
this purpose, microbiological gas production30,31 is mobilized as capacity to precipitate CaCO3 .34,35
a means of desaturation via production of biogenic gas bubbles CaCO3 is found to precipitate in three main polymorphs:
to achieve an overall increase in liquefaction resistance. vaterite, aragonite and the much more stable calcite.36 These
Such innovative concepts have an important effect on the CaCO3 phases exhibit different shapes, geometries and solubility,
greater geo-engineering field both from a research and industrial with vaterite being spherical and highly soluble and calcite cubic
point of view. Firstly, they defy established practices by bringing and less soluble.37,38 Environmental conditions such as tempera-
into surface alternative mechanisms, with some of them mobi- ture, pH and pressure are considered to affect the precipitating
lizing processes which are found in nature to serve as examples polymorph as well as transitions to metastable phases.

Please cite this article in press as: Terzis D. and Laloui L., A decade of progress and turning points in the understanding of bio-improved soils: A review, Geomechanics
for Energy and the Environment (2019), https://doi.org/10.1016/j.gete.2019.03.001.
D. Terzis and L. Laloui / Geomechanics for Energy and the Environment xxx (xxxx) xxx 3

An aspect of the mechanism of soil bio-improvement, with process of bacterial attachment on soil grains to ultimately induce
controversial interpretations found in the literature, refers to the growth of calcite cubic particles is presented in a schematic
the role which microorganisms hold in the precipitated CaCO3 approach in Fig. 1. Apart from this schematic representation,
polymorph. Whilst the mechanism of MICP is widely appreci- insight into the real geometries of calcite bonds is provided in
ated as bio-mediated precipitation, some results indicate that Fig. 251 where cubic particles of CaCO3 are captured via Scanning
there exists dependency, at least for the initial polymorph which Electron Microscopy (SEM). Hierarchical expansion of the bigger
precipitates, on the microbial agent responsible for urea hy- particle surfaces is observed, with planes found to reproduce
drolysis. A study performed by Wei et al.36 compares CaCO3 those of individual calcite crystals observed in their vicinity.
precipitation kinetics and morphologies induced by the ureolytic Fig. 352 presents an assembly of soil grains bound by calcite
Sporosarcina, Bacillus and Brevundimonas species. The precipitated particles, all exhibiting similar sizes and geometries, captured via
CaCO3 polymorphs are found to depend both on environmental SEM.
conditions39,40 and to preferable polymorph precipitation by the Depending on the desired final CaCO3 content, the quick over-
adopted ureolytic gene.41,42 all reaction times of MICP can range from several hours to a few
The debate over the suitability of ureolysis-driven calcite pre- days, thus rendering the technique a feasible solution for modern
cipitation as soil strengthening technique is intensifying with engineering applications. Moreover, another advantage of MICP
respect to ammonium, a side-product of urea hydrolysis. De- is the reduced energy requirement for in-situ applications, which
spite the belief that ammonium can be captured and recycled implies reduced overall application costs. This is attributed to the
through loops of recirculating reactants, concerns over residual low viscosity and increased workability of the employed bacterial
ammonium have led to the development of alternative concepts. and reactive solutions. Lower pressures are required for their
Among them we find denitrification using calcium acetate and propagation via infiltration through granular media, instead of
calcium nitrate.43,44 Despite successful applications based on den- mixing highly pressurized fluids with soils. MICP is thus widely
itrification being reported, low reaction rates are believed to appreciated as a non-intrusive, permeation mechanism which
represent a major challenge, if not the bottleneck of the process, leaves the initial soil state intact during deposition and growth
which remains to be overcome towards application of denitrifi- of calcite bonds upon introduction of reactive species. The need
cation in realistic timeframes in conventional construction and of extensive injection repetitions is avoided since MICP offers
geotechnical problems. the ability to generate flow networks to circulate bacteria and
An alternative concept to improve efficiency of future in- reactants and thus improve larger soil volumes through few in-
situ applications based on calcite mineralization relates to bio- filtration steps. A further sign of the economic efficiency of the
stimulation of native calcifying species.45,46 This strategy bypasses process lies in recirculating the utilized water during infiltration
the direct introduction of ureolytic bacteria into the ground by of the targeted volume. This allows, on one hand, reducing the
providing necessary nutrients and conditions for native species volume of water needed for dissolving reactant elements and, on
to grow and induce precipitation of calcium carbonate bonds. the other hand, performing quality control tests on the effluent
An advantage of bio-stimulation is the reduced risk of causing solutions and capturing produced NH4 + , a by-product which is
unwanted clogging of pores due to accumulation of bacterial widely used as fertilizer in agricultural applications.
cells, since these latter are not injected directly into the ground, To fully understand the overall performance of MICP, one
but grow gradually and homogenously due to nutrient-rich en- should account for the improvement in the obtained mechanical
vironments. However, preliminary quality control analyses are properties of the bio-treated geo-material, in relation to the mass
required in the area of foreseen applications to identify native of products used to achieve the targeted bond content. MICP
species and to adapt accordingly stimulation strategies which is reported to yield cohesion values in the range of hundreds
target the favoured growth and metabolic activity of calcifying of kPa51 and values of compressive strength in the absence of
strains against all other native species. A recent study by Gat confinement above 10 MPa.53 More importantly, the desired level
et al.47 deals with the effect of MICP on the indigenous bac- of improvement can be determined and controlled according
terial population composition of coastal sand samples collected to the nature of the foreseen geo-engineering application. For
from a semi-arid environment in Israel, which yielded low initial example, MICP can be designed to endow the targeted material
ureolytic potential. The study introduces organic carbon to bios- with cohesion values in the range of 50–60 kPa to increase its
timulate indigenous, ureolytic species and provides with evidence resistance against liquefaction. Alternatively, MICP can be im-
of nitrification during the period following application of MICP, plemented for producing materials with strength and stiffness
where ammonia oxidation occurs. values close to those of typical concrete, which allows considering
earth materials for structural purposes. The technique’s greatest
3. Microbially Induced Calcite Precipitation (MICP) advantages are its adaptability and flexibility in the design of
the final soil improvement solutions for tailoring, at will, desired
To date, the term cementation has been associated with the in- material properties in a given area of interest.
troduction of artificially manufactured cementitious mixtures and The technique has been studied in a series of frameworks
industrial fluids in the subsurface. MICP induces a peculiar type which require different levels in calcite bond contents. Below,
of soil cementation with calcium carbonate acting as cementing a summary of problems considered suitable for implementing
element. The reactive mechanism at its core is urea hydrolysis solutions based on MICP is presented with reference to relevant
with the catalyzing activity of the urease enzyme Eq. (1), which is works:
found in several bacterial strains.48 Fujita et al.49 firstly reported
on the correlation between the rate of calcium carbonate precipi- i. Improve soil mechanical properties for securing the
tation and that of urea hydrolysis. Among urease-bearing species, necessary bearing capacity45,54
Sporosarcina pasteurii,50 a bacterium isolated from soils, is found ii. Bio-clogging; a term used to describe the clogging of
to yield the highest urea hydrolysis rates. pores for mitigating leakages in reservoir formations or the
Moreover, due to their wall electronegativity, S. pasteurii cells construction of underground barriers55–58
attach on soil grains where they induce urea hydrolysis and iii. Slope stabilization59,60
release CO3 2− in their micro-environment. There, precipitation iv. Mitigating liquefaction risk61,62
of CaCO3 occurs under the presence of a calcium source. This v. Fugitive dust control63

Please cite this article in press as: Terzis D. and Laloui L., A decade of progress and turning points in the understanding of bio-improved soils: A review, Geomechanics
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Fig. 1. Schematic representation of S. pasteurii cells (black) attaching on soil grains (brown dodecahedra) and inducing the formation and growth of calcite cubic
particles (white); system of grains (top) and porous assembly of soil grains (bottom).132

Fig. 2. Particles of CaCO3 captured via SEM revealing hierarchical expansion of planes (arrows) for bigger bond particles, which reproduce the geometries of
neighbouring single crystals (circles); black arrows indicate traces of bacteria encapsulated on the crystals’ contact plane with sand grains.51

Please cite this article in press as: Terzis D. and Laloui L., A decade of progress and turning points in the understanding of bio-improved soils: A review, Geomechanics
for Energy and the Environment (2019), https://doi.org/10.1016/j.gete.2019.03.001.
D. Terzis and L. Laloui / Geomechanics for Energy and the Environment xxx (xxxx) xxx 5

Fig. 3. Calcite particles (arrows) binding sand grains.52

vi. Production of masonry and bio-bricks23,64 ultimately obtain samples at the desired dimensions, which can
vii. Erosion protection65 , targeting slopes and river banks66 be subsequently subjected to mechanical loading.72 The advan-
viii. Vegetation applications related to soil erosion67 tage of this approach is that complex sample coring is avoided.
ix. Stabilization of tunnelling walls68 This technique allows testing lower bond contents as reported in
x. Increasing soil thermal conductivity52 the work by Montoya and DeJong.73 Finally, medium scale (0.5
xi. Land reclamation69 m diameter) tanks are used by Cheng59 as a means of obtaining
larger bio-cemented volumes to core samples for mechanical
testing. Overall, homogenous calcite distribution at laboratory
4. State of the art scale would imply reliable experimental data sets, as far as the
mechanical response is concerned, and would facilitate compari-
The characterization of the behavioural characteristics of the son between results produced in various studies. Detecting calcite
bio-improved geo-material at laboratory scale is treated here in distribution remains a challenge with various approaches sug-
detail. Interest is further put on studies which up-scale MICP gested towards accurate and representative measurements51,74 at
to evaluate overall feasibility of the bio-cementation mechanism the scale of conventional geotechnical testing.
towards providing solutions to real-world problems. Next, we A principal difference between MICP and traditional cemen-
dedicate a section to studies developed around multi-physical tation mechanisms for soils is that soil structure remains intact
modelling of the complex biological, chemical and hydraulic throughout treatment by infiltration. Therefore, the initial pack-
phenomena coupled in MICP. Except for notions of multiphysi- ing of grains holds a governing role on the formation of the final
cal modelling, the review extends to incorporate studies which lattice of bonds. The effect of initial dry density on the obtained
address the behaviour of bio-improved soil in constitutive mod- mechanical response was treated in the work by Chou et al.70
elling frameworks. Finally, works developed around the numeri- for low calcite contents that yielded peak deviator stresses in the
cal study of the bio-improved geo-material are presented with a range below 50 kPa. van Paassen53 reports values of unconfined
compressive strength (UCS) between 1–12 MPa. He concludes
focus on the use of the Discrete Element Method (DEM).
that soils with lower initial relative density require increased
mass of bond contents to reach similar strength with respect
4.1. The bio-improved geo-material at laboratory scale
to the same material which was treated via MICP under ini-
tially higher relative densities. A hypothesis is that calcite bonds
Specimen preparation processes are reported covering vari-
precipitate preferably around the contact points of grains. Thus,
ous set-ups and applied conditions to ultimately produce bio- denser initial states correspond to larger number of contact points
improved specimens. The overall challenge in each case is no among particles, as shown schematically in Fig. 4. Attention
other than the homogeneity in the samples’ calcite distribution. should be made on the way the calcite bond content is expressed.
Typically, specimens are produced in cylindrical moulds using This can be done in terms of volumetric fraction, for example, of
peristaltic pumps to introduce reactive elements either via batch the total soil volume or with respect to the fraction of the solid
(stop-flow) or continuous flow. One peculiar preparation method phase. It is easily understood that looser initial states correspond
was conducted by Chou et al.70 who placed sand samples in to increased fraction of pores per given soil volume thus bond
permeable moulds within a reservoir and applied continuous agi- contents expressed in terms of fraction of the solid phase can
tation for recirculating dissolved elements through the permeable be considerably higher with respect to denser initial states. In
cloth. Another approach is reported by Keykha et al.71 who used this direction, Mahawish et al.75 established a correlation be-
electrodes for distributing reactants, i.e. dissolved ions of calcium tween strength and stiffness of coarse sand with the increase in
and urea, throughout sand columns by generating an electric the amount of deposited CaCO3 , initial relative density and dry
field to drive carbonate dianions (CO3 2− ) and calcium cations density.
(Ca2+ ) across the length of the columns. Moreover, a different MICP is widely treated as a cementation mechanism targeting
approach suggests circulation of bacteria and chemical reactants shallow depths and thus most available results report the me-
within specimens placed in triaxial cells, under confinement, to chanical behaviour of treated soils in terms of UCS. Fewer results

Please cite this article in press as: Terzis D. and Laloui L., A decade of progress and turning points in the understanding of bio-improved soils: A review, Geomechanics
for Energy and the Environment (2019), https://doi.org/10.1016/j.gete.2019.03.001.
6 D. Terzis and L. Laloui / Geomechanics for Energy and the Environment xxx (xxxx) xxx

Fig. 4. Schematic representation of contact points and bond (grey) repartition for minimum (left) and maximum (right) relative dry densities; white lines represent
intergranular contacts and idealized intergranular force transmission.

are available for triaxial drained tests under confinement or for Common agreement is found among researchers as far as
one-dimensional oedometric compression. In this direction, some the effect of treatment conditions on the obtained fabric and
relevant work is reported by Feng and Montoya,76,77 Fauriel68 and mechanical properties of MICP-treated soils is concerned. More
Terzis and Laloui.78 Additionally, while the material is considered precisely, among such parameters reported in the literature are
to yield tensile strength, few attempts have been made towards environmental conditions, concentrations of biological and chem-
quantifying this parameter. Li et al.79 report results on the effect ical elements, the speed and direction of the imposed reactive
of the presence of fibres on the overall tensile strength of sand flow field. Because of varying treatment conditions the geome-
stabilized via MICP and van Paassen53 presents results of Brazilian tries and overall spatial distribution of CaCO3 bonds are found
tensile strength (BTS) tests, with values reaching up to 500 kPa. to be affected. More precisely, Al Qabany and Soga85 reported
As far as the permeability of the material is concerned, results increasing UCS for increasing dry density of MICP-cemented spec-
suggest80–82 that the hydraulic conductivity reduces up to one imens. Results obtained in this latter work attempt to highlight
order of magnitude. In addition, Kirkland et al.83 performed low- the role of chemical factors in the geometrical and spatial dis-
field nuclear magnetic resonance to detect changes in porosity. tribution of crystals and associate this role with the obtained
They conclude that the final porosity is in the range of 85% of the engineering properties of the material. Somewhat surprisingly,
initial value, which was measured prior to application of MICP, for the larger crystals observed after injection of 1 mol/litre (M)
with the rest porous space occupied by calcite. Contrary, clogging of CaCl2 , no increase in UCS was reported for any calcite content.
of pores refers to the intentional calcification around the vicinity Indeed, these samples were reported not to exhibit homogenous
of an injection source or within fissures in rock formations. Such cementation and the cemented volume was limited to the vicinity
attempt is reported by Cunningham et al.55 for ultimately sealing of the injection point. Such evidence suggests that there exists
fractures and mitigating leakages in well-bores. a series of factors, determined based on the decision-making
A confusing point in the literature relates to the characteriza- around the provided treatment, which reflects to distinctive ge-
tion of the level of cementation within produced samples. Terms ometries and distribution of the bond lattice. These geometries
such as light or heavy cementation appear in several studies and lead to varying post-treatment mechanical response, regardless
are associated with bond contents as low as 3%. However, it of the base material chosen for treatment. More studies81,86,87
is commonly appreciated that contents below 3% fail to endow have attempted to further capture the effect of treatment condi-
materials with the necessary mechanical integrity under uncon- tions on the overall MICP efficiency by providing with qualitative
fined conditions for laboratory experimentation. For example, van descriptions of observed precipitate behaviours. The effect of
Paassen53 reports the highest range of CaCO3 content found in environmental factors was investigated on the bio-cementation
literature between 12%–24%. These latter results allowed estab- of coarse sand by Mahawish et al.88 who found that the optimal
lishing a trend between the precipitated mass and the expected conditions for the bio-cementation of their adopted base material
range of strength. Montoya and DeJong73 showed that calcite is reactant concentration of 1 mol/L at 20 ◦ C.
contents as low as 1% lead to increase in shear strength, under Cheng et al.80 introduced a simple way for performing in-
undrained conditions, with respect to the untreated material at jections by allowing reactants to flow into columns through
loose state. In this same work, the achieved range of calcite infiltration from the surface. Results showed significant variation
content (1.3%) is characterized by authors as moderate cemen- of the obtained UCS values for samples of the same calcite con-
tation. It should be noted that tests, in this case, were ran at an tent. Calcite was found to be more efficiently distributed and lead
initial confinement of 100 kPa, followed by increase in the mean to increased UCS for conditions where soil is partially saturated
effective pressure due to excess pore water pressure generation. with reactant solutions during treatment. This is attributed to
Thus, understanding the specific conditions under which samples liquid menisci that form around the grains and maintain reactants
are tested is important towards evaluating the overall calcite – and thus precipitated nuclei – around the crucial grain-to-grain
content, and therefore its classification within the low-moderate- contact points. This was the first study to demonstrate that CaCO3
heavy cementation spectrum. Overall, results available in the crystals, which were formed under lower degrees of saturation,
literature refer to a variety of CaCO3 contents, ranging from 0.6 exhibited more efficient distribution around the areas of desired
and 1.2%84 to 25%.53 Contents that might appear very low, such as crystal deposition, i.e. contact points among grains. Such distinc-
contents lower than 2%, can indeed endow the desired, improved tive particle deposition is considered to contribute to increased
properties to geo-materials, given the role of confinement in strength of the cemented samples for lower calcite contents. A
problems of geo-technical interest. schematic representation of this hypothesis is presented in Fig. 5.

Please cite this article in press as: Terzis D. and Laloui L., A decade of progress and turning points in the understanding of bio-improved soils: A review, Geomechanics
for Energy and the Environment (2019), https://doi.org/10.1016/j.gete.2019.03.001.
D. Terzis and L. Laloui / Geomechanics for Energy and the Environment xxx (xxxx) xxx 7

Fig. 5. Schematic representation of bonds precipitating within the liquid phase for 100% saturation conditions (left) and within liquid menisci at lower degree of
saturation (right).

No further results are available in the literature regarding the summarized in Table 1, which were produced under different set-
effect of the degree of saturation during MICP-treatment on the ups, targeting different calcite ranges and using various quantities
post-treatment mechanical response. This might be attributed to to capture and describe the improved mechanical response.
the complex control of the degree of saturation in granular ma- More precisely, Table 1 summarizes a series of key findings
terials with poor water retention capacity. However, the finding reported in the literature in representative studies during the last
itself, based on the hypothesis of more efficient bond distribution decade. This summary illustrates the range of calcite contents
yielded due to liquid menisci, serves as another example of the achieved and the variety of conditions tested to characterize
importance of controlling external factors which hold strong ef- mechanical and physical properties of bio-improved soils.
fect on the obtained mechanical response. Results obtained from From the studies presented in Table 1, specific focus is put
UCS tests in the same study by Cheng et al.80 show that for on strength and stiffness, cohesion and friction properties as well
partially saturated conditions (Sr = 20%) same level of strength as on hydraulic conductivity.65,80,85 Comparison is also done with
(in the range of 3 MPa) is reached at only one third of the total other cemented materials, such as gypsum-cemented sands.93 For
bond content required for specimens which were MICP-treated calcite contents above 3%, UCS values are commonly reported,
under fully saturated conditions. since samples maintain their integrity without the application
Considering the above, there exists a series of external factors of confining pressure. Contents up to 27%54 endow sands with
that need to be meticulously chosen and controlled in order properties that resemble those of building materials. However, as
to achieve efficient application of MICP. However, the role of previously discussed in this paper, MICP is herein studied from a
intrinsic properties of the base material subjected to MICP on geotechnical perspective and therefore the role of confinement
the properties of the calcite lattice remains to be understood. needs to be understood in relation with the targeted calcite con-
While most studies refer to sandy soils treated under MICP, less tent. Contents as low as 2% can therefore be sufficient to improve
is known about the effect of grain size distribution or that of mechanical properties, to satisfy safety factors and to meet the
fine content of the base material, with most recent the contri- required bearing capacity limits.
bution from Zamani and Montoya89 on the undrained monotonic The role of confinement is further understood in Fig. 6, which
shear response of MICP-treated silty sands. Along similar lines, presents the response of two different base materials under three
Nafisi and Montoya74 proposed a framework which accounts for confining pressures (30, 100, 200 kPa). Maximum peak deviatoric
the particle size effect on bio-cementation of sands. Gomez and stress reaches shy of 2800 kPa for medium-grained sand under
DeJong90 compared various types of sands with fine contents 200 kPa of confinement. Duraisamy93 reports experimental data
up to 13% subjected to MICP while Cardoso et al.91 investigated on triaxial drained tests for MICP-treated sand of calcite contents
the role of clay contents reaching 28% on the MICP process. All up to 7.3%, with peak deviatoric stress reaching 2600 kPa under
the above works highlight the critical role the base materials’ 50 kPa of confinement. It should be noted that this latter work
intrinsic properties hold in the resulted mechanical response adopts sand of a mean diameter (D50 ) equal to 0.39 mm as base
and bio-improved fabric. In a similar attempt to provide with material. Similar sand is adopted by Terzis and Laloui78 which
quantified data on the evolution of the mechanical properties and yields peak deviatoric stress equal to 2500 kPa under 30 kPa of
of the micro-structure of bio-improved soils, Terzis and Laloui78,92 confinement (Fig. 6). Both studies conclude that the effect of bio-
compare the behaviour of two types of sand of different grain cementation is more pronounced for lower values of confinement.
size distribution which were subjected to MICP under identical As another example of this key finding, Table 1 reports a range of
external treatment conditions. Samples yielded overall calcite 1437–1870 kPa for the peak deviatoric stress yielded by samples
contents between 7%–8%. Results are summarized in Figs. 6 and 7, of 4.2% calcite content under confinements of 50 kPa and 500 kPa
and reveal that medium-grained sand yields considerably higher respectively.
peak strength under drained conventional triaxial compression A comprehensive summary of six studies presenting experi-
and under unconfined compressive strength tests, despite similar mental results on the UCS of bio-improved sands was presented
response of the two materials in their untreated state (Fig. 6). in the review work by El Mountassir et al.94 Fig. 8 is enriched
Therefore, it becomes clear that the average calcite content with recent data from Mahawish et al.95 on coarse-grained bio-
cannot serve as the sole indicator of the expected, improved me- cemented sand. A distinctive trend is established by Terzis and
chanical behaviour of the bio-treated state. This is critical towards Laloui92 as far as the evolution of UCS of medium-grained sand
interpreting literature results of bio-treated soils, such as those (D50 = 0.39 mm) is concerned, compared to fine sand (D50 =

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8 D. Terzis and L. Laloui / Geomechanics for Energy and the Environment xxx (xxxx) xxx

Fig. 6. Mechanical response for untreated (dashed) and MICP-treated (solid) fine- (grey) and medium-grained (black) sand; (top) deviatoric stress versus axial strain;
(bottom) normalized specific volume versus axial strain.

Fig. 7. Unconfined compressive strength for fine- and medium-grained MICP-treated specimens (a); evolution of the Young’s modulus for fine- and medium-grained
bio-improved sand with respect to increasing bond content (b).

0.19 mm), which is found to validate the trend of the rest of the result to the formation of precipitates. In such an attempt, Singh
literature works. et al.98 provided with a micromodel of a porous medium to study
Recent literature studies report results from undrained triaxial the precipitation evolution at the micro-scale using the bacterial
shear tests. Cui et al.96 performed tests for bio-improved samples strain Pseudomonas stutzeri.99 The above approaches, bring the
which reached 11.87% in calcite content. Results reveal a peak research focus to the smallest scale possible, studying particle-
deviatoric stress of 2750 kPa for the maximum calcite content to-particle or cell-to-particle phenomena and can serve towards
achieved (11.87%) and an effective cohesion which reaches just robust upscaling of microscopic phenomena which were treated,
below 450 kPa. until recently, through a series of hypotheses.
Moving beyond conventional geo-technical testing, we notice
that the bio-improved geo-material offers research challenges 4.2. The challenge of up-scaling
related to micro-mechanical testing. Montoya and Feng97 inves-
tigated particle crushing between calcite grains in contact and Several field-scale applications have been reported that tar-
bond-breakage evolution during shearing to determine whether get the bio-cementation of larger volumes of fine-grained sandy
MICP bonds experience cohesive or adhesive failure. They per- soils,54 or stabilization of sands to mitigate fugitive dust45,63,100
formed surface energy measurements and studied particle-bond- and apply MICP to field experiments in gravels.101 All these stud-
particle deformation patterns coupled with electron microscopy ies provided crucial findings related to the overall feasibility of
to conclude that the failure mechanism is rather of cohesive MICP at large experimental scale, such as the distribution of cal-
nature. Microscale experimentations do not limit to the study of cite content over a large soil volume, and further revealed several
mechanics. Transport phenomena can capture real-time data and challenges for the application of an efficient and reproducible soil
reveal critical information on the involved mechanisms which improvement process that was based on MICP.

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for Energy and the Environment (2019), https://doi.org/10.1016/j.gete.2019.03.001.
D. Terzis and L. Laloui / Geomechanics for Energy and the Environment xxx (xxxx) xxx 9

Table 1
Overview of key findings reported in the literature on mechanical and physical properties of bio-improved soils.
Source CaCO3 (%) range Strength Stiffness quantities Other Remarks
reported
van Paassen et al.54 12–27 0.7–12 MPa (UCS 1300–13 000 MPa c′ = 280–540 kPa 100 m3 experiment
and triaxial) (Eur ) ϕ ′ = 39–58◦ (fine sand)
Cheng59 4.5–11.5 (coarse) Up to 2067 kPa – – 2 m column
0–27.5 (fine) (UCS coarse) up to injection
3700 kPa (UCS fine)
Cheng et al.80 1–14 150–2300 kPa (UCS) 20–180 MPa (E) k-valueb in the same MICP under various
order of magnitude degrees of saturation
Al Qabany and 0–8 Up to 3000 kPa – One order of Same base
Soga85 (UCS) magnitude reduction material/different
in k-value treatment conditions
Feng and Montoya77 1.4/3/5.3 280–800 kPa (qmax , – c′ = 5–59 kPa ϕ ′ = Injections directly in
loose/moderate/heavya σ3′ = 100 kPa) 33–41◦ triaxial cell
Lin et al.72 1–2.5 400 kPa Up to 250 MPa (Ei , – Two types of sand
(σ3′ = 100 kPa) tangent (Janbu, adopted 20/30 and
1968)) 50/70
Duraisamy93 0.26–9.34 50–950 kPa (UCS) Up to 1350 MPa qmax = Comparison with
(small-strain shear 1437/1870 kPa for gypsum cemented
modulus Gmax ) σ ’3 = 50/500 kPa samples
and CaCO3 = 4.2%
Jiang and Soga65 0–1.4 – – One order of Application for
magnitude reduction erosion control in
in k- value gravels
(10−4 m/s)
Terzis and Laloui92 3%–10% Up to 11.3 MPa E up to 1950 MPa Quantified Two types of sand
(UCS) microscopic data adopted: D50 = 0.19
mm and D50 = 0.39
mm
- Results not available.
a
Characterization of the level of cementation.
b
Hydraulic conductivity.

Fig. 8. UCS evolution with respect to CaCO3 content.


Source: adapted and enriched with repsect to94 ,
including results from129–131 .

More precisely, van Paassen53 performs MICP treatment in remaining in the range around 500 kPa. At a subsequent attempt,
1 m3 and 100 m3 experiments. The resulted volume allowed van Paassen101 applies MICP in field conditions, to an area with
for coring samples which are considered to exhibit homogenous gravels, targeting the stabilization of the soil substrate prior to ex-
calcite distribution at laboratory scale. Results reveal UCS values cavation and installation of a pipeline. This application confirmed
above 10 MPa and values of Young’s modulus up to 13 GPa. the presence of mineralized CaCO3 ; however, no bio-cemented
This latter test was duplicated under similar conditions and with samples were further obtained for testing. Gomez et al.63 per-
the same base material by Filet et al.102 with results for UCS formed MICP via surface percolation in an in-situ application

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10 D. Terzis and L. Laloui / Geomechanics for Energy and the Environment xxx (xxxx) xxx

in Californian desert (USA), where the goal was to cement the X-ray computed tomography as a means of calibrating their nu-
upper crust of the targeted area, for ultimately providing evidence merical transport model and estimating the radial precipitation
towards the efficiency of MICP for mitigating fugitive dust. Re- of, CaCO3 , extending this way the predictive modelling of MICP
sults show that a cemented crust was formed of about 2 cm in in the three-dimensional space. Recently, Nassar et al.107 pre-
depth. Focusing on the impact of environmental factors towards sented a complete modelling approach which uses zero fitting
upscaling MICP, Mortensen et al.103 reported that their biological parameters to simulate and predict bio-stimulation in a 1.7 m
treatment shows robust efficiency over various soil types, which diameter tank. Results showed good agreement with the actual
were adopted as base materials, and water compositions referring experiment which was ran in the tank, where 3 injection wells
to varying concentrations of ammonium chloride and salinity were employed.
levels. Such attempts suggest that a crucial step prior to upscaling It becomes clear that such modelling attempts require cali-
is considering the properties of the in-situ base material and per- bration with experimentally measured parameters for a robust
form feasibility studies under laboratory conditions. Moreover, prediction of the final mass of calcite and its spatial distribu-
continuous monitoring of the reaction process is necessary, as tion. Such an attempt was provided by Lauchnor et al.108 on
a means of obtaining real-time data sets corresponding to key whole cell kinetics of urease hydrolysis using S. pasteurii. This is
factors related to the evolution of precipitation and MICP effi- possible only in the case of large-scale tests, provided that the
ciency. Such real-time quality control can take place via collection experimental set-up is equipped with the necessary monitoring
and analysis of effluent volumes or via geophysical methods to systems. Martinez et al.109 provide a similar framework for MICP,
monitor density change due to bio-cementation. where theoretical prediction of reactive transport and kinetics
These works at the larger experimental scale further reveal of ureolysis are addressed, including mass of precipitated CaCO3
the need of a new approach, as far as the utilization of urease and urease activity. More precisely, obtained parameters were
and the conception of a reproducible application mechanism are calibrated against experimentally measured values in a 0.5 m
concerned. A common reference between all these attempts is column test. Results revealed good agreement with theoretically
the need to cultivate bacteria cells at the site of application. predicted parameters. However, authors in this latter work agree
Thus, bioreactors need to be built, with the provision of agitation that complexity in predictions will increase when parameters
systems for incubating bacterial cultures which often becomes a such as bacterial growth or reactive transport in the 3D domain
complicated task. In this direction, a cell-free approach of MICP enter the problem. Similar conclusions are derived in the work by
has been studied in Terzis and Laloui.92 The main finding is that Barkouki et al.110 where a bio-geo-chemical model is developed
urea hydrolysis and calcite precipitation persist in a cell-free en- to capture precipitation kinetics and transport phenomena for
vironment, after complete breakdown of rehydrated bacteria that the case of batch treatments (stop-flow as mentioned by the
were prepared in dry-powder form. The use of freeze-dried cells authors) and continuous flow in MICP induced by S. pasteurii.
as inoculum is considered to facilitate in-situ application of MICP In this latter work, the imposed flow regime and time allowed
and contribute to overall reproducible soil bio-improvement between batches for precipitation to occur are found to affect the
applications and subsequent quality control. Similar finding re- homogeneity in calcite distribution.
garding the persistence of urease, which maintains its ureolytic As an example of the increased complexity of the actual
activity in the absence of viable cells, were reported by Mortensen phenomena involved in MICP, we consider that as calcification
et al.103 In this study cell lysis occurred due to anoxic conditions progresses, bacterial cells get trapped in the precipitated nuclei
and the enzyme was believed to keep hydrolysing urea, for an and left deprived of oxygen and nutrients. Thus, they do not
unknown time, till its ultimate degradation. contribute to further hydrolysis. Moreover, the presence of gas
bubbles alters considerably flow regimes. As discussed in the
4.3. Multi-physical modelling work by Cheng et al.,80 partially saturated conditions can in-
duce more efficient distribution of calcite particles altering the
The processes involved in MICP offer researchers with chal- relationship between calcite content and mechanical response.
lenges that are related to multi-physical modelling. How far can The existence of a design approach which quantifies parameters
bacteria travel from a given injection source? What is their activ- such as hydrolysis rates, decay of bacteria, as well as crucial
ity during continuous recirculation of reactants and what is the environmental conditions would allow predictive modelling to
final distribution of calcite along the imposed flow path? take place on a more representative basis with respect to the
Researchers have attempted to provide answers towards physical mechanisms of MICP which have been captured and
addressing these uncertainties by bringing notions of reactive- reported experimentally.
transport processes together and addressing involved couplings
with the use of analytical methods. This is possible by accounting 4.4. Constitutive modelling
for phenomena such as attachment of bacterial cells, their rate
of growth, decay and their efficiency to hydrolyse urea, among The bio-improved geo-material’s peculiar structure would
others. Such progress unifies the contributing factors of MICP classify a potential attempt to address its behaviour in a mod-
and allows for predictive modelling as far as the final mass and elling framework in the grey area between rock and soil me-
distribution of calcite within porous media are concerned. At a chanics. The fabric of bio-improved soils does not resemble that
second stage, the precipitated mass of calcite can be introduced of naturally cemented soils or artificially cemented soils yielded
as a parameter to mechanical constitutive modelling to finally upon application of jet grouting, for example. This is due to
predict the behavioural characteristics of the material. Fauriel and distinctive geometries of the binding element, i.e. CaCO3 , and
Laloui104 developed a numerical tool based on Michaelis–Menten varying trends in bond sizes and spatial distributions reproduced
kinetics for the reaction process. The model was implemented according to applied treatment conditions.
for two configurations, one that simulates the application of Fauriel68 implemented a theoretical model to capture the
MICP under a system of existing buildings and a second which performance of bio-improved soils by extending the constitutive
simulates stabilization of the walls of a tunnelling excavation.68 concept that was developed for unsaturated aggregated soils by
Relevant parameters have been studied in numerical simulations Koliji et al.111 to account for the effects of bonding and density
by Dupraz et al.105 among which variations in pH and calcite change. The main features of this proposed framework are the
precipitation. Akimana et al.106 coupled reactive modelling with incorporation of a hardening variable, to account for the effects

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D. Terzis and L. Laloui / Geomechanics for Energy and the Environment xxx (xxxx) xxx 11

of the apparent overconsolidation due to the density change characteristics to different phases of the solid skeleton. Except
upon precipitation and the incorporation of a destructuration for the peak strength further, focus by researchers has been
parameter to govern the post-yield softening behaviour of the put on the post-yield behaviour. Such relevant work is reported
geo-material. However, the physical significance of these param- by Jiang et al.122 who performed 2D DEM numerical analyses
eters remains unclear and their conception and calibration are focusing on the degradation evolution in cemented geo-materials
based on a series of back-analysis prediction of experimental by providing, in addition, with microscopic interpretation of the
data available in the literature. This model, however, did set the underlying mechanisms.
basis for addressing the behaviour of MICP-treated soils within For the specific case of bio-improved soils, except for multi-
the critical-state concept. The main features reproduced are the physical modelling where coupled bio-chemical and transport
elastic response upon initial yielding, post-yield softening and a phenomena are addressed in a unified framework, a series of
residual condition which represents the response of the com- works treating their behavioural characteristics is reported using
pletely destructured state. As widely reported by researchers, numerical tools.97,123–125 As concluded by Evans et al.123 the prin-
bio-improved materials yield brittle failure in the small-strain ciple of parallel bonds, widely applicable in DEM simulations of
region. Though, less is known about the underlying mechanisms granular materials, is not considered representative for the case of
and the contribution of dilatancy in the peak strength. bio-improved soils. This happens due to the vanishing of individ-
Cheng et al.80 in their work on MICP under partially saturated ual particles when their strength limit is reached, which implies
conditions implement a mechanistic model on a simplified ge-
that mass conservation is not respected. For larger cementitious
ometry to account for the volumetric fraction of bonds yielded
particles, which better reflects the case of bio-improved soils,
during application of MICP at various degrees of saturation. A sta-
Evans et al.123 provide with a more robust design of the 3D
tistical analysis captures the evolution of bond diameters and the
packing geometry. They introduce cementitious bonds in chain
way they affect changes in porosity. Therefore, physical insight is
formations and conclude that parameter calibration needs to be
provided offering tangible evidence on the geometry of the lattice
done, with the sizes of bonds considered as crucial parameter
of bonds. This work sets the basis for expressing the evolution
governing the overall response. Recently, Yang et al.125 treat the
of microstructural quantities with respect to the evolution of the
case of very low calcite contents in the range of 0.6% in DEM
calcite bond content. Despite its simplified approach based on
idealistic geometries of grains, it reflects the principle of bond simulations. The main finding relates to understanding the con-
growth upon continuous deposition of precipitated nuclei. tribution of inter-particle friction and increasing shear resistance
Nweke and Pestana112 introduced a strength correlation which to the dilation and re-arrangement of the packing structure in
takes into account nonlinearities of failure envelopes observed in an attempt to interpret the macro-scale response with respect
bio-cemented sands. In the suggested approach, the strength of to particle-scale phenomena. Finally, notions of contact stiffness,
the bio-improved material is expressed as a function of post-MICP contact mechanics and inter-particle friction126 are incorporated
density, applied confinement and by accounting for the material’s in such approaches to ultimately express the improved structure
intrinsic mineralogy. and understand the chain force distribution within the solid
Similar materials which exhibit bonded structures could in- matrix, a term commonly confronted in DEM simulations.
spire further progress in modelling the behaviour of MICP-treated
soils. For example, gas-hydrate bearing soils113–115 are studied by 4.6. Insight into the micro-scale
incorporating formulations to account for the different hydrate
particle habits, as a means of expressing structural characteristics While new understanding around the geometries and spatial
in the adopted modelling approaches based on the critical state distribution of the CaCO3 crystals within the new improved struc-
concept. This approach was extended to capture the case of bio- ture has been reported, relevant works which became available
improved soils in a recent work by Gai and Sánchez116 which
until 2016 have provided only with qualitative description of
incorporates a critical state yield surface, sub-loading concepts
microstructural properties. What we know so-far about calcite
and also accounts for bond degradation. Efforts to model the
crystalline bonds is that they develop their structures follow-
behaviour of microbially-cemented soils resulted in a modelling
ing hierarchical plane expansion, like the ones shown in Fig. 2,
formulation proposed by Gajo et al.117 which incorporates micro-
but how large they eventually grow remains undetermined. A
scale inspired parameters. More precisely, cross-scale functions
hypothesis adopted by the authors is that increased contact
are introduced to express a relationship between the evolving
area between bonds and grains results into lower intergranular
microscopic variables and the resulting macroscopic material
stresses. Among the questions that remain to be answered is
behaviour. These parameters refer to the reactive surface area,
how these bonds increase their diameters and how bond sizes
cross-sectional area and the number of bonds for materials which
experience dissolution or precipitation. This model was success- vary with respect to the intrinsic properties of the base material
fully validated against experimental data provided by Montoya and the final overall calcite content. Relevant work towards ad-
and DeJong.73 The same experimental data series were used by dressing these uncertainties was provided recently in Dadda et
Gai and Sánchez116 to validate their proposed model. al.127,128 and Terzis and Laloui.92 In this latter work, a workflow
is presented which incorporates X-ray micro-computed tomog-
4.5. Numerical modelling raphy and 3D volume reconstruction to capture and analyse the
critical contact area and a series of micro-scale parameters.
Numerical simulations, especially through implementation of To understand the importance of such findings one should
Discrete Element Method (DEM) codes, have facilitated sig- consider the role of fabric anisotropy in sands. Particle sizes,
nificantly the study of the behaviour of packings of grains shape and orientation influence the behavioural characteristics
with bonds,118 as well as the statistical analysis of micro- of natural sands and are all related to sample preparation. Rel-
scopic quantities, such as size of grains, number of contacts and evant works explore these effects for various types of sand.119,120
orientations,119–121 all found to affect the overall mechanical However, an approach to quantify microscale parameters of the
response of granular materials. The main advantage of such MICP-improved soil fabric remains to be determined. This task
analyses lies in the ability to reproduce different packings and ge- seems challenging because of the fabric anisotropy induced by
ometries of grains and bonds and attribute strength and stiffness the applied bio-treatment conditions to the porous material.

Please cite this article in press as: Terzis D. and Laloui L., A decade of progress and turning points in the understanding of bio-improved soils: A review, Geomechanics
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12 D. Terzis and L. Laloui / Geomechanics for Energy and the Environment xxx (xxxx) xxx

5. Towards mainstream engineering applications on MICP: (i) complete correlation of the material foreseen to
be improved with the chosen bio-treatment strategy, (ii) stan-
Are we ever going to witness a mainstream geo-engineering dardized and reproducible treatment methods where strategies
application based completely on bio-mediated processes? This to introduce bio-cementation agents and treat by-products are
question is continuously involved in the branch of geotechni- meticulously designed and monitored and finally, (iii) a design
cal engineering studied in the present review. To offer tangible method which targets and achieves the mass of calcite bonds to
evidence, and thus treat this question on a less philosophical ultimately meet desired mechanical properties.
and more pragmatic approach, there is need to provide with
a robust description of the processes involved in the problem. Acknowledgements
Processes which start from the moment calcifying bacterial cells
The authors express their sincere thanks to the Swiss Na-
flow within the porous medium and mineral deposition oc-
tional Science Foundation (SNSF) (grant 200021_140246) and
curs, until the formation of the final structure and subsequent
Swiss Federal Commission for Scholarships for Foreign Students
deformation under mechanical loading. Most importantly, an-
(Swiss Government Excellence Scholarship ESKAS-Nr: 2014·
swering the above question requires multidisciplinary approach
0276) for their financial support. Additionally the authors would
and cooperation among experts who treat problems of varying
like to acknowledge the support of the Lombardi Foundation
nature.
(Switzerland).
Common agreement is established among researchers sug-
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Please cite this article in press as: Terzis D. and Laloui L., A decade of progress and turning points in the understanding of bio-improved soils: A review, Geomechanics
for Energy and the Environment (2019), https://doi.org/10.1016/j.gete.2019.03.001.
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