Perspective

Received: 30 May 2014

Revised: 18 July 2014

Accepted article published: 25 July 2014

Published online in Wiley Online Library: 14 August 2014

(wileyonlinelibrary.com) DOI 10.1002/jctb.4502

The use of carbonic anhydrase to accelerate

carbon dioxide capture processes
Joel K. J. Yong, Geo W. Stevens, Frank Caruso and Sandra E. Kentish*
Abstract
The chemical absorption of CO2 into a monoethanolamine solvent is currently the most widely accepted commercial approach to
carbon dioxide capture. However, the subsequent desorption of CO2 from the solvents is extremely energy intensive. Alternative
solvents are more energy ecient, but their slow reaction kinetics in the CO2 absorption step limits application. The use of a
carbonic anhydrase (CA) enzyme as a reaction promoter can potentially overcome this obstacle. Native, engineered and articial
CA enzymes have been investigated for this application. Immobilization of the enzyme within the gas absorber or in a membrane
format can increase enzyme stability and avoid thermal denaturation in the stripper. However, immobilization is only eective
if the mass transfer of carbon dioxide through the liquid phase to reach the immobilization substrate does not become rate
controlling. Further research should also consider the process economics of large-scale enzyme production and the long-term
performance of the enzyme under real ue gas conditions.
2014 Society of Chemical Industry
Keywords: Carbon Capture; Enzymes; Mass Transfer; Membranes

INTRODUCTION

J Chem Technol Biotechnol 2015; 90: 310

Correspondence to: S.E. Kentish, Department of Chemical and Biomolecular

Engineering, The University of Melbourne, Parkville, VIC 3010, Australia. E-mail:
sandraek@unimelb.edu.au
Department of Chemical and Biomolecular Engineering, The University of
Melbourne, Parkville, VIC, 3010, Australia

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2014 Society of Chemical Industry

The emission of carbon dioxide (CO2 ) into the atmosphere is

of great concern today because these emissions create environmental issues that are associated with global warming.1 CO2 is a
greenhouse gas that traps infrared radiation from the sun within
the atmosphere and prevents it from escaping, which ultimately
causes the Earth to become warmer over time. The signicant
growth in CO2 emissions is mainly derived from human industrial
activities2 such as thermoelectric power plants, cement plants and
steel plants. A report from the European Commission estimated
the quantity of CO2 emitted into the atmosphere to be approximately 34 billion tonnes in 2011,3 with these emissions set to
increase over the next few decades. These CO2 emissions have
caused problems with weather patterns around the world and,
according to the fth assessment report from the Intergovernmental Panel on Climate Change (IPCC)4 , strong action is required if we
are to maintain a sustainable living environment.
Many attempts have been made to reduce the CO2 emissions
from human activities to counteract the undesirable eects of
climate change. Carbon capture and storage (CCS) technologies1
are engineering solutions which target the capture of CO2 that
is produced from major emitters such as fossil fuel-red power
plants. This carbon dioxide can then be stored underground in
geological formations such as deep saline aquifers or disused
hydrocarbon reservoirs,5 or precipitated as carbonates that are
environmentally benign.6
Carbon dioxide is an inert and unreactive molecule that is thermodynamically stable, which makes it dicult to capture and separate. In addition, the concentration of CO2 within incoming power
station ue gases is only approximately 414 vol%, which adds to
the diculty.7 A large variety of approaches to this problem have
been reviewed, including the use of physical adsorption,8,9
membranes,10 12 cryogenics13 and hydrate formation.14,15

However to date, the most eective approach to this intransigent

problem has focused on the use of chemical absorption of CO2 by
liquid solvents. The solvent that is most commonly considered is
monoethanolamine (MEA) which has been well characterized over
the years.1,8,9,16 This solvent is extremely eective in forming stable
carbamates when reacted with CO2 , leading to a very ecient
removal of CO2 in a 2:1 reaction stoichiometry.9,17 19 However,
regeneration of the carbamate species 17 requires a large parasitic
supply of energy to release the CO2 during stripping.8,9,20,21 This
high energy requirement accounts for up to 80% of the operating
costs.22
There are a number of other solvents under consideration for
carbon capture, including hindered and tertiary amines, chilled
ammonia and potassium carbonate (K2 CO3 ). While many of these
solvents are able to reduce the stripping energy requirement,
the reaction rate for CO2 sorption in the absorber is often slow.
This means that it is not possible to recover high purity carbon
dioxide within a reasonable column height. Carbonic anhydrase
(CA) is a naturally occurring enzyme that is known to catalyse
the conversion of CO2 into bicarbonate (HCO3 ) at extremely high
turnover rates, which may be useful for promoting the absorption
rates of CO2 from gas streams when these alternative solvents
are used.7 There is great potential for using CA to hydrate CO2 ,
especially when it is known that the hydration step is the rate
limiting step in the CO2 absorption process. This paper focuses
on the development of CA as a catalyst and its ability to function

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under industrial operating conditions. The paper includes a review
of the current technologies that are being used for CO2 absorption
and how they may be signicantly enhanced by the addition of CA
as a catalyst.

JKL Yong et al.

been investigated thus far.24,39 This application forms the basis of

the remainder of this paper.

CARBONIC ANHYDRASE
SOLVENT ABSORPTION PROCESSES
FOR CARBON CAPTURE

In a typical carbon capture process, ue gas is fed to the bottom

of a tall column. The gas stream is contacted with a liquid solvent
stream that ows from the top of the column to the bottom
of the column. The absorption of CO2 is usually conducted at
temperatures of 3050 C.21,23 Packing media are placed within
the column to promote contact between the gas and the solvent
for more eective absorption. The CO2 -rich solvent can then be
sent to a regenerator that is operated at 120140 C9 to recover
the CO2 for purication and storage, while the stripped solvent can
then be pumped back into the absorber for reuse. A schematic of
the CO2 absorption/desorption process is shown in Fig. 1.
While MEA is the most commonly considered solvent for
post-combustion capture of CO2 , it is also a highly corrosive
substance1,7,24 that readily undergoes degradation in the presence of oxygen,9,16,18 emits harmful volatile organic compounds
(VOCs),16 and its high relative volatility requires that frequent
replenishment of the solvent is necessary.25 Further, as indicated
above, the energy demand associated with solvent regeneration
is signicant.
Sterically hindered amines such as 2-amino-2-methyl-1-propanol
(AMP) and tertiary amines such as N-methyldiethanolamine
(MDEA) require much less energy for regeneration and have
a higher CO2 capacity because they react with CO2 at a 1:1
stoichiometry; however, their reaction rate is slow, relative to
MEA.16,19,26 These solvents are also known to be less volatile
than MEA, which also limits the rate of solvent loss during the
operation.27
Ammonia has also been reviewed as a solvent for the absorption of CO2 , having demonstrated a noticeably lower operating
energy requirement than the alkanolamines,28 where the reaction between ammonia and CO2 follows a single-step termolecular
mechanism.29 There is also a possibility for the absorption products (mainly ammonium carbonate) to be used as soil fertilizers to
minimize the overall production of waste.28 However, the absorption reaction kinetics for ammonia are again signicantly slower
than that of MEA.
Potassium carbonate (K2 CO3 ) solutions have been used at industrial scale for CO2 absorption in the Beneld process.30 Again,
there is signicant evidence that the operating energy requirement is lower than that of alkanolamine absorption20 because the
HCO3 ions that are produced upon the absorption of CO2 into
K2 CO3 require less energy for regeneration than the carbamates
produced from MEA.31,32 Sodium carbonate/bicarbonate systems
have been considered for similar reasons.33 However, these solvents again exhibit slower rates of CO2 absorption compared with
the alkanolamine solvents when operated under the same conditions.
For each of these alternative solvents, a promoter or catalyst is
required to increase the absorption rate of CO2 .21,30,31 A wide range
of materials that can be used as promoters for aqueous solvent
absorption has been investigated, including boric acid,31 arsenic
acid,34 piperazine35,36 and amino acids.37,38 Carbonic anhydrase
(CA) is also often considered as a promoter, as it has been shown to
be more eective as a catalyst than the other promoters that have

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CA is a metalloenzyme that regulates important biological processes within humans and other living organisms such as the
acidbase balance within the blood,40 the photosynthesis mechanism in plants41 and the carbon concentration mechanism in
microorganisms.41 It is dened by the Enzyme Commission (EC)
Number 4.2.1.1 and can be further classied under ve dierent categories (, , , and ) based on its structure and its
origins.2,42 44 The most commonly investigated class of CA is the
form,45 which is generally found in mammals. In -CA, the enzyme
acrtivity is derived from a Zn2+ ion that is coordinated to three histidine residues near the centre of the molecule in a cone-shaped
cavity (Fig. 2).46 -CA predominates in plants and algae and is
also found in Bacteria and Archaea. In this case, the Zn2+ ion is
co-ordinated to two cysteine residues and one histidine residue
on the protein.47 While -CA is always present as a monomer, -CA
exists as dimers, tetramers, hexamers, and octamers. Conversely,
-CA is mostly present in single cell micro-organisms (Archaea) and
always exists as a trimer.47 Iron- and cobalt-substituted forms of
this -CA exhibit greater CO2 hydration rates than the zinc enzyme
and it is possible that the enzyme functions using such transition
metals in place of zinc.47 Conversely, -CA, which is extracted from
diatoms, has Cd2+ as the metal ion catalyst, reecting the lack of
Zn2+ available in a marine environment.48 It can be said, though,
that the enzyme is more ecient at CO2 hydration when the Cd2+
ion is replaced with Zn2+ .49
The hydration of CO2 occurs when the Zn2+ ion abstracts a
proton from a surrounding water molecule, creating a hydroxide
ion that is negatively charged and can attack the partially positive
carbon atom on a solubilised CO2 molecule to form a HCO3 ion1,39,47,50,51 This mechanism is shown in Fig. 3 for an -CA:
The reaction mechanism can also be summarized in Equations
(1) and (2):1,39,47,50,51
+
2+

Zn2+ + H2 O

H + Zn OH

(1)

2+

Zn2+ OH + CO2

Zn + HCO3

(2)

The overall reaction rate for this process can be approximated

by:1
([
] [
] )
k
rCA = cat [CA] CO2 CO2
Km
where kcat is referred to as the turnover number and ranges
between 104 and 106 molecules of CO2 per molecule of CA per
second depending upon the organism.2,39,45,47,52,53 The specicity
constant, kcat /Km is reported to be approximately 108 M1 s-1 ; 53
Russo et al.54 obtain a specicity constant of 9.16 106 M1 s1
for a thermally stable recombinant carbonic anhydrase at 25 C
while Alper and Decker record a value of 0.90 L mg1 s1 at 25 C
with an activation energy of 9.0 kcal mol1 at a pH range of 9.6 to
11.1.55
This Zn2+ ion is also capable of catalysing ester hydrolysis, such
that various researchers have developed a standard assay for quantifying the activity of CA based on the hydrolysis of p-nitrophenyl
acetate.21,43,52 However, the activity of CA in ester hydrolysis may
not correlate with the activity of CA in CO2 hydration and is

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Carbonic anhydrase to accelerate carbon dioxide capture processes

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Figure 1. Schematic of a solvent absorption process, based on a solvent such as monoethanolamine (MEA).

(a)

(b)

(c)

Figure 2. Ribbon diagrams of typical -, -, and -class carbonic anhydrase crystal structures. Active site zinc ions are shown as red space-lled spheres;
monomer subunits in the - and -class carbonic anhydrases are individually coloured. (a), -class, human isozyme II, 30 kDa; (b), -class, Escherichia coli,
dimeric unit of the native tetramer, 98.8 kDa; (c), -class, Methanobacterium thermophila, 69 kDa. Figure reproduced with permission from Tripp et al.47

usually lower in the hydrolysis reaction than it is in the hydration

reaction.56 It has also been mentioned that CA also promotes the
formation of CaCO3 ,6 which may be useful when considering the
storage of CO2 as insoluble carbonates instead of in its pure form.
However, the precipitation of carbonates presents a separate issue
with regards to the procurement of appropriate cations for the formation of the insoluble carbonates.

ENGINEERING CA FOR THE ABSORPTION

OF CO2

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If most native CA strains were to be exposed to the operating

temperatures within a solvent absorptions process, especially in
the stripper stage, they would undergo denaturation extremely
readily. Indeed, it is known that most CA strains lose their activity between 55 and 65 C.57,58 However, thermostable CA strains
have been found in thermophilic microorganisms32,42,59 and have
also been produced in engineered recombinant microorganism
strains.60 These strains can tolerate temperatures of 8090 C,
which make them useful as catalysts if they can be retained in the
absorption stage.
The CA enzyme must also be tolerant to other components that
are found within the inuent gas feed. The ue gases that are emitted from power plants contain a mixture of sulphur and nitrogen
oxides,16 which can also inhibit the activity of the CA. The activity of
CA has been found to be inhibited by a wide variety of anions,2,42,61
including NO3 at concentrations as low as 0.05 mol L1 .2 However,
the concentration of such anions is unlikely to reach this level in
most capture processes, particularly if there is upstream ue gas
desulphurization. Bond et al.52 show that there is little indication

of inhibition at the concentrations that might be expected in such

situations (i.e. below 100200 mmol L1 of SO2
or NO3 ). Simi4
larly, Lu et al. nd that concentrations of up to 0.9 mol L1 SO2
,
4
0.2 mol L1 NO3 and 0.7 mol L1 Cl did not inuence the kinetics
of absorption from a CA loaded potassium carbonate solution62 .
An alternative to genetic engineering of CA strains is the manufacture of articial enzyme mimics. These mimics generally
involve the use of a Zn2+ ion bound to various ligands. The
most active small molecule CA mimic identied thus far is the
1,4,7,10-tetraazacyclododecane chelate of zinc(II) perchlorate,
referred to as zinc cyclen (Fig. 4).57 This molecule has a ve-fold
lower activity than the native enzyme on a mass basis, but is
commercially available on a large scale.57 Furthermore, it has been
shown that zinc cyclen can retain its activity at temperatures of up
to 75 C and to retain its structure up to 100 C, suggesting that
it will survive passage through a standard CO2 stripping cycle.57
The catalyst is inhibited by signicant bicarbonate concentrations,
which drive the reverse reaction in Equation (2). However, this inhibition can be overcome by maintaining a high pH in the absorber
(>9), in order to minimize this bicarbonate concentration.57 A
range of similar macrocyclic tetraamine zinc complexes have been
identied as CA mimics.63 65
Other species which have been shown to mimic the action of CA
include a zinc-histadine complex,66 a zinc-imidazole complex7,67
and a poly(N-vinylimidazole)zinc complex.51 Zastrow et al.68 construct an articial metalloenzyme that includes a three-stranded
coiled coil containing both a catalytic metal site, ZnN3 O and a
separate HgS3 site for structural stabilization. They claim that this
approach provides a simplied construct that retains sucient
complexity to resemble a native protein environment.

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JKL Yong et al.

Figure 3. CO2 hydration mechanism of carbonic anhydrase. Figure reproduced with permission from Zhang et al.50

Figure 4. Zinc cyclen perchlorate, which can act as an eective CA mimic,

consists of a hydrated zinc atom coordinated to a cyclic amine ligand.
Reproduced from Floyd et al.57 with permission.

ENZYME IMMOBILIZATION

The immobilization of an enzyme to a solid substrate is a focal

point for research because it aids the reuse of the enzyme and
lengthens its lifespan.69 Immobilization has also been shown to
improve the thermostability of various types of enzymes.23,70 72
In addition, with the immobilization of the enzymes within the
absorption stage of the process, there is no need to expose them
to the harsher temperature conditions within the stripper, which
also helps to prolong their operational lifespan.
There have been reports of CA enzymes being immobilized
onto activated carbon particles,21 polyurethane foams,43,59
silica nanoparticles,23,73,74 silica beads,75 chitosan,71 chitosan
and silica coated magnetic particles66 and gold nanoparticles
functionalized with silica.76 A wide array of methods have been
used for immobilising CA onto the abovementioned surfaces,
including the use of hydrogels,50,77,78 covalent bonding through
reaction with aldehydes73 or with cyanogen bromide and
triethylamine,79 cross-linked aggregation,73 physical adsorption,73
and layer-by-layer (LbL) electrostatic adsorption.80 A structural analysis of human CA adsorbed onto silica nanoparticles

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showed that the active site was not signicantly disrupted upon
adsorption,74 which indicates that most of the enzymatic activity
can be preserved after it has been immobilized.73,76 In other cases
immobilized CA demonstrated a decreased activity relative to free
CA,73,75 but immobilization was shown to improve the thermal
stability21,81 and the half-life of CA,23,82 which led to an increased
operating lifespan.
However, when CA is immobilized onto a solid support, the
resistance to the mass transfer of the carbon dioxide through the
liquid phase to reach this support can often be rate limiting.83 This
limits the eectiveness of the catalyst.1,84 Indeed, Penders-van Elk
et al. argue that this means that enzyme immobilized onto xed
packing material within a classical packed column will never be
eective.85 To resolve this issue, some workers have considered
the use of a trickle spray ow over enzyme-immobilized packing,41
while others have considered the immobilization of CA onto
ne particles which can more readily penetrate the gasliquid
interface.86 Only when the particle size in the resulting slurry
reduces below 10 microns in size does the turnover number
approach that of the free enzyme (Fig. 5).

THE USE OF CARBONIC ANHYDRASE

IN MEMBRANE CONTACTORS
Drawbacks of the use of packed columns such as those shown
in Fig. 1 are the high capital cost and the requirement for a
large footprint for placing these columns.9,87 More recently, the
use of gas membrane contactors has been investigated, as these
can have a larger surface area to volume ratio.88,89 The approach
reduces the material requirements for construction signicantly,
and uses a smaller footprint area.90
In the simplest case, referred to as membrane gas absorption (MGA) the solvent ows through the shell side of a hollow bre membrane bundle, while the ue gas moves through

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Carbonic anhydrase to accelerate carbon dioxide capture processes

Figure 5. The turnover factor (ToF), relative to that calculated for free
enzyme, as a function of the average particle diameter used for enzyme
immobilization. The dashed line is a rough indication of the trend. Reproduced with permission from Penders-van Elk et al.85

Figure 6. The principle of membrane gas absorption. Reproduced with

permission from Yan et al.96

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Figure 7. Schematic of contained liquid membrane (CLM) operation. The

solvent is immobilized within the membrane pores. This solvent may
incorporate CA.

membrane, lling the pore space (Fig. 7). One surface of this
membrane is contacted with the feed gas, so that the CO2 diuses
into the liquid phase encapsulated within the membrane.39 The
other surface is contacted with a sweep gas, which draws the
dissolved CO2 out of the liquid phase for purication. A CLM thus
combines the absorption and desorption process within a single
modular setup, which eliminates the need for expensive columns
and reduces the overall capital cost. A variation of the CLM is a
hollow bre contained liquid membrane (HFCLM) where two sets
of hollow bres are packed together into a single microporous
hollow bre permeator. The solvent is contained in the spaces
between these bres (shell side). The ue gas is then passed
through the lumen of one set of bres while the sweep gas is
passed through the lumen of the other set (see Fig. 8).
It was established 40 years ago that the presence of CA within
such a liquid membrane enhanced the mass transfer ux of CO2
across the membrane, with a CO2 reaction rate that was proportional to the quantity of CA present within the membrane.100 More
recently, the performance of CA, DEA and NaHCO3 for CO2 removal
was compared when used in a CLM. It was concluded that CA was
the most eective at removing CO2. 18 The system also demonstrated potential for scaling up to treat industrial ue gases.101
Borchert and Saunders showed that the eciency of a HFCLM with
a free CA concentration of 0.6 g L1 in a 1 mol L1 sodium bicarbonate (NaHCO3 ) solution could dramatically improve the absorption rate of CO2 based on a continuous CO2 feed concentration of
15%.60 However, other workers have shown that a CLM is unable
to maintain a long-term stable performance over the longer term
as the CA that is dissolved in the liquid denatures and loses its
CO2 hydration activity. These authors argue that it is more prudent to immobilise the CA within the membrane in a hydrogel
phase.50 Carbozyme also immobilise the enzyme in a HFCLM format, with the CA immobilized to the external walls of the hollow
bres, to ensure that the incoming CO2 contacts the enzyme at the
gasliquid interface (see Fig. 8).101
In an alternative approach, Yao et al.51 immobilized a
polymeric-metal CA mimic as a thin polymeric lm on a porous
support. In this case, there was no solvent phase. Rather, the
humidication of the feed and sweep gas was sucient to allow
the CA mimic to facilitate the transport of the carbon dioxide as it
passed across the membrane.

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the bore or lumen side of each bre. The hydrophobic microporous membrane acts as a barrier that prevents liquid transfer, but allows for the transport of carbon dioxide, as shown
in Fig. 6. A separate hollow bre membrane contactor is used
for the stripping operation.91 Common hydrophobic materials
that are used as membrane contactors include polypropylene
(PP),87,92 96 polyvinylidene diuoride (PVDF),97 99 polytetrauoroethylene (PTFE)87,92,93 or PP that has been coated with PTFE.94
Arazawa et al. considered the covalent immobilization of CA onto
the liquidgas interface of polymethylpentene membranes in an
MGA format to gauge the suitability of the membranes as articial
lungs for removing CO2 from blood. These authors showed that
the removal rate of CO2 from the blood was 36% greater for membranes with immobilized CA than for membranes without CA.79
However, more research has been focused on contained liquid
membrane (CLM) contactors. In a CLM setup, the absorption
solvent, containing CA, is immobilized within the microporous

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JKL Yong et al.

REFERENCES

Figure 8. Conceptual diagram for operation of the Carbozyme Permeator,

which uses CA immobilized on the external surface of hollow bre membranes in a HFCLM format. Reproduced from Trachtenberg et al.101 under
a Creative Commons license.

DISCUSSION AND CONCLUSIONS

With the use of CA as a promoter in the absorption process,

less toxic and more energy ecient solvents such as K2 CO3 can
be used instead of MEA. Most research to date has focused on
the eectiveness and energy eciency of this approach. However, if this enzyme is to be used at an industrial scale, the
research needs to now shift to address three key issues. First,
the thermostability of the enzyme must be enhanced at a realistic cost. Common CA sources such as bovine CA or human
CA lack resilience at conventional CO2 absorption process temperatures and even less so at desorption conditions. Frequent
replacement of the enzyme to maintain the CO2 removal rates
would become prohibitively expensive, not only because of the
enzyme cost, but because of the excessive downtime from capture
operations.
Borchert and Saunders have obtained a thermostable form of
CA from a recombinant E. coli bacterial strain,61 but there is a high
capital cost associated with the large-scale production of enzymes
from such recombinant E. coli cell lines.104 Even though Migliardini et al. argue that there are available technologies to produce
enzymes from recombinant cell lines at moderate cost,60 these
costs are generally not included in the process economics of operating a CA-based CO2 absorption process. A cost analysis on the
use of enzymes for the production of lignocellulosic ethanol has
shown that there is a signicant cost attached with using enzymes
in the pretreatment step;105 hence it can be expected that a thermostable CA would also contribute a signicant cost component
towards the operation of CA-facilitated CO2 absorption processes.
The use of an enzyme mimic such as zinc cyclen may provide
a cheaper alternative and more work is recommended to fully
understand the economics of this alternative.
Second, more work needs to be conducted to characterize the
operating lifespan of both native CA and the enzyme mimics, particularly after immobilization. The performance of these molecules
in absorption columns or membrane contactors must be assessed
over periods of months or years, not the hours or days characteristic of most laboratory experiments. Long-term resilience to ue
gas contaminants and process variations in temperature, pressure
and owrate is yet to be fully tested.
Finally, the enzyme is only eective when acting at the
gasliquid interface, as the liquid phase resistance to mass transfer otherwise becomes rate controlling.86 Therefore, research
needs to focus on methods of immobilization that locate
the CA in this position, if true reaction enhancement is to be
achieved.

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