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REVIEW ARTICLE
1Department of Neuroanaesthesia, National Hospital for Neurology and Neurosurgery, Queen Square,
London WC1N 3BG, UK. 2Department of Medical Physics and Bioengineering, University College London,
Capper Street, London WC1E 6JA, UK. 3Academic Department of Anaesthesia, University College London
Hospitals, Middlesex Hospital, Mortimer Street, London WC1N 8AA, UK
*To whom correspondence should be addressed
in cerebral haemodynamics and oxygenation at the bedside. When light of a known wavelength is used to transilluminate
Near infrared spectroscopy (NIRS) has been used for this a solution of a compound of unknown concentration in vitro,
the extinction coefficient and thickness of solution traversed
purpose for many years in neonatal intensive care and has
can be substituted in the Beer–Lambert equation to derive
the potential to be a monitor of cerebral well-being in
the concentration of the substance. Spectroscopy in this
adult intensive care and anaesthesia, particularly in the
form has been used for many years in colorimetric analysis
neurosciences. Although the principles underlying its use are
and, in certain circumstances, similar principles can be
relatively straightforward, they are often poorly understood.
applied to biological tissue.
This review presents an overview of the physical prin-
ciples involved in the measurement of tissue oxygenation Biological absorbers
with NIRS and describes how it may be used to continuously
Visible light (wavelength 450–700 nm) does not penetrate
observe changes in cerebral haemodynamics and oxygen-
biological tissue to a thickness greater than approximately
ation. The clinical experience with NIRS is described in
1 cm because it is strongly attenuated as a result of powerful
addition to the techniques for non-invasive measurement of
absorption and scattering by the tissue constituents. One of
cerebral blood flow (CBF) and cerebral blood volume the most significant absorbers of light is water which also
(CBV). has a strong absorption at wavelengths of more than 900 nm.
However, there is a window of wavelengths in the near
infrared region between 650 and 900 nm in which photons
Physical principles
are able to penetrate tissue far enough to illuminate deeper
Absorption of light by coloured compounds structures such as the cerebral cortex.9 47 In addition, there
are compounds in the tissues whose absorption of light
Light passing through a solution of a coloured compound
varies with their oxygenation status. In the near infrared
(or chromophore) is absorbed by the compound and the
range, oxyhaemoglobin (HbO2), deoxyhaemoglobin (Hb)
intensity of the emerging light is therefore reduced. The
and oxidized cytochrome oxidase (CytOx) have character-
relationship between the concentration of a chromophore,
istic absorption spectra.69 The concentrations of HbO2, Hb
c, its extinction coefficient a (which describes the optical
and CytOx are likely to change rapidly during alterations
characteristics of a compound at a given wavelength), the in cerebral perfusion and oxygenation, and a technique
thickness of solution, d, and the ratio of incident to emergent allowing real-time measurements of these changes might
Io find a place as a monitor of cerebral well-being. The
light intensity is given by the Beer–Lambert equation:
I potential of NIRS as a non-invasive monitor of cerebral
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Owen-Reece et al.
calculation used to solve the modified Beer–Lambert equa- converts the changes in light attenuation to changes in
tion at each of these wavelengths is known as an algorithm. chromophore concentration. Beyond this stage, two distinct
Several algorithms have been published and these vary methods of data handling can be described. They are
depending on the wavelengths of light used, presence of fundamentally different but frequently confused and data
other chromophores and the precise values for absorption from the two methods are often presented as though they
coefficients chosen.28 58 67 Recent work has applied different were interchangeable. The performance of two commer-
published algorithms to the same data set and revealed cially available spectrophotometers using these different
striking differences in the calculated concentration approaches has recently been compared.48
changes.42 It is clearly important that the algorithm is known
when NIRS data, collected using different equipment, are (1) Non-quantitative measurements—cerebral
presented. oximetry
Although the absorption coefficient for CytOx is approxi- Cerebral saturation can be measured using techniques which
mately twice as great as that for haemoglobin, the tissue avoid fully quantifying changes in haemoglobin concentra-
concentration is at least one order of magnitude less.60 The tion. The INVOS 3100 (Somanetics, MI, USA) measures
signal from CytOx is also more dependent on the algorithm the ratio of light absorption by HbO2 and HbT, and from
than that from haemoglobin and for this reason too, caution it calculates a value for mean cerebral saturation, thus
must be used in interpreting NIRS-derived CytOx measure- avoiding quantification of change in haemoglobin concentra-
ments. In comparison, the signal for haemoglobin is much tion. Human studies using the first commercial version were
more robust. published in 1991.45 46 The technique uses a two-wavelength
near infrared source, emitting light which is detected by
Comparison of NIRS with pulse oximetry two receivers. In the original version, one was at 1.0 cm
Confusion often occurs in respect of differences between and the other 2.7 cm from the light source. The transmitter
NIRS and pulse oximetry. There are three fundamental and receivers are arranged in a linear fashion such that the
differences. light arriving at the proximal receiver is considered to have
(i) Different wavelengths are used in the two techniques passed largely through non-cerebral surface tissues whereas
and NIRS therefore has far greater tissue penetration than the distal receiver detects light also passing through brain
pulse oximetry. tissue. If the signal received by the proximal receiver is
(ii) Pulse oximetry deliberately considers only the arterial subtracted from that of the distal receiver, the ratio of the
compartment by time gating the measurements. It calculates two gives a mean value for cerebral oxygen saturation.
the ratio of HbO2 to (Hb1HbO2) on the pulsatile component McCormick and colleagues demonstrated that it was pos-
and displays it as SpO2. NIRS does not discriminate in this sible to measure regional cerebrovascular oxygen saturation
way and provides a global assessment of oxygenation in with this arrangement.45
all vascular compartments (arterial, venous and capillary). Others have had some difficulty in replicating these
(iii) NIRS uses more wavelengths for spectroscopic transil- results. For example, Harris and Bailey produced an increase
lumination and can therefore characterize more chromo- in middle cerebral artery blood flow velocity measured
phores than pulse oximetry. using transcranial Doppler by inducing hypercapnia, but
were unable to demonstrate a change in regional cerebral
oxygen saturation.27 Similarly, Lewis and co-workers38
Equipment design demonstrated that regional cerebral oxygenation measured
There are a variety of commercially available equipment by the INVOS did not reflect significant changes in cerebral
which allow tissue spectroscopy. It should be noted that oxygenation detected by the global measurement of jugular
there is a difference in the manner in which NIRS is applied venous bulb oxygen saturation (SjO2). These results are
to measure cerebral changes in neonates and adults. In difficult to explain but may be a result in part to inadequate
neonates, the thin skull and small head allows light to be inter-optode separation. In a study during carotid angio-
shone through the whole head and transmission spectro- graphy, four receivers were placed on the scalp at separations
scopy is possible. In adults however, the large head and thick from the transmitter of 1.5, 2.5, 3.5 and 4.5 cm. When a
skull require reflectance spectroscopy where the transmitting bolus of the infrared absorber indocyanine green was
and receiving optodes are placed a few centimetres apart injected into the internal carotid artery, relative absorption
on the same side of the head. The algorithms used to increased with detector distance from the light source but
derive chromophore concentrations are equally valid for no substantial difference in attenuation was observed in any
measurements made in both situations. of the detectors during external carotid injection.31 Direct
There are basic features common to all commercially DPF measurements have also shown that with inter-optode
available NIRS equipment. Light is generated at specific distances of less than 2.5 cm, it cannot be assumed in adults
wavelengths by laser photodiodes which can be detected that DPF will have a predictable value, as with small inter-
either by a photomultiplier tube (PMT)7 or, in more recent optode spacings the surface tissues have a disproportionate
equipment, by a silicon photodiode.5 32 A computer then effect on light transport and light will not reliably penetrate
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Near infrared spectroscopy
the cortex.65 As most of the near infrared light travels along also been demonstrated that it is possible to measure changes
an extracranial path when the source–detector separation is in CBV in response to alterations in PaCO2 in adults53 and
less than 2.5 cm, it is important to use the maximum inter- during cardiopulmonary bypass in children.18 Changes in
optode spacing compatible with adequate light detection. cerebral haemodynamics with varying end-expiratory pres-
In adults, an inter-optode spacing of 4 cm is now typically sure,16 tilting41 and induction of anaesthesia40 have also
used by most investigators. been documented. Furthermore, neurological status after
Cerebral saturation values measured with the INVOS cardiac surgery has been compared with intraoperative
have been compared with SjO2.24 These authors recorded a measurements of cerebral oxygenation.50 Cerebral haemo-
change in cerebral oxygen saturation of 3.6% for every dynamic changes measured by NIRS have been correlated
10% change in SjO2 and also confirmed that extracranial with peripheral oxygen desaturation, intracranial hyperten-
tissues had a negligible effect on cerebral saturation values. sion and cerebral hyperaemia in a group of head-injured
Finally, in a pragmatic approach to the problem of variability patients.35 NIRS was able to detect correlated changes in
of the value for cerebral oxygen saturation provided by the 97% of events whereas SjO2 registered changes in only 53%.
INVOS, Schwartz and colleagues made measurements in The authors commented on the apparent high sensitivity of
18 dead subjects.61 They found that mean saturation was NIRS compared with SjO2 monitoring. Finally, it has been
51 6 27% compared with 68 6 5% in a group of normal demonstrated that intrapartum changes in fetal Hb, HbO2
healthy controls. Six of the 18 dead subjects had a value and HbT concentrations can be monitored effectively using
greater than the lowest values for healthy adults. As the an NIRS probe attached transvaginally to the fetal head.1 57
algorithms for the INVOS are not published, it is difficult NIRS apparatus allowing quantification of changes in
to make meaningful comparisons with data generated by haemoglobin concentration can also be used to calculate
other equipment. cerebral saturation in a variety of ways. One approach is
A newer version of the INVOS, with a larger source– to induce brief, small changes in CBV by digital occlusion
detector separation (3–4 cm), is now available and greater of one jugular vein.72 The resultant changes in HbO2
sensitivity to intracerebral events is claimed. Work with this concentration can be divided by the changes in HbT
equipment has demonstrated that scalp ischaemia induced by concentration to give a measure of cerebral haemoglobin
a pneumatic tourniquet results in a decrease in measured saturation during the period of blood volume change. Two
regional cerebral oxygen saturation, suggesting that the studies have compared measurements at different values of
inbuilt compensation for the effect of extracerebral tissues arterial oxygen saturation17 or arterial PaCO2.56 A particular
is still inadequate.23 However, this study confirms that when advantage of measuring cerebral saturation with this method
scalp ischaemia is established, cerebral saturation varies is that being a ratio of two concentrations, the variable is
with arterial saturation, suggesting sensitivity of the device free of the potential errors introduced using a differential
for intracranial events. This apparatus has also been used pathlength factor.
successfully to detect cerebral hypoxia during carotid endar- Another NIRS system which provides an absolute meas-
tectomy,68 but others have failed to show a relationship urement of tissue haemoglobin saturation has been described
between regional cerebral saturation measured by the recently.43 The spatially resolved spectrometer (SRS)
INVOS and jugular bulb oximetry in comatose patients incorporates several detectors housed in a single probe
after cardiac arrest.6 which is placed 4–5 cm from the source. Combination of
these multi-distance measurements of optical attenuation
(2) Quantitative concentration measurements with the usual multi-wavelength spectroscopy data allows
The second category of NIRS equipment allows full quanti- calculation of the relative concentrations of Hb and HbO2
fication of changes in chromophore concentration and in the illuminated tissue and therefore an estimate of mean
maximizes the potential of tissue spectroscopy. Equipment tissue haemoglobin saturation. It is possible to follow trends
allowing this has been developed by several manufacturers, in cerebral oxygenation with this apparatus although it
including Hamamatsu Photonics (Hamamatsu City, Japan), appears to underestimate the absolute mean cerebral satura-
Critikon (Ascot, Berkshire, UK) and Radiometer tion compared with other methods.17
(Copenhagen, Denmark). These quantitative data, although Finally, absolute cerebral saturation may be measured
from an unknown baseline, have formed the basis for using a phase shift technique. If laser light oscillating at a
several studies. Early clinical studies, which did not take known frequency is used to transilluminate the head, the
account of pathlength, observed changes in cerebral HbO2, emerging light is out of phase with the incident light. This
Hb and CytOx concentrations in adults20 and neonates19 phase shift is directly proportional to the actual pathlength
and in these same chromophores during skeletal muscle of light through the tissue sample and is wavelength specific.
ischaemia.26 Subsequently, several studies which incorpor- Such phase shift measurements allow absorption and scat-
ate DPF have been carried out. These demonstrate that tering to be quantified and calculation of absolute changes
changes in cerebral haemodynamics in preterm infants in cerebral HbO2 and Hb concentrations and saturation.36
can be observed after alterations in arterial PaCO271 and One clinical study has attempted to correlate changes in
administration of indomethacin12 and surfactant.13 It has cerebral saturation measured by this method with the onset
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occlusion of the jugular vein, as described above,72 is more flow to the NIRS signal, Owen-Reece and colleagues
likely to be comparable with changes in jugular venous measured CBV in nine adults before and after inflating a
oxygen saturation. pneumatic tourniquet proximal to the NIRS measurement
There has also been considerable speculation on the area site.55 Because a change in scalp blood content could
of brain, both topographically and functionally, that is being potentially change the pathlength of light passing through
interrogated by NIRS. Computer modelling can demonstrate the head, the optical pathlength was also measured before
the area of brain illuminated and has shown that this is and after tourniquet inflation. Occlusion of scalp blood flow
subject to significant influence from fluid–tissue interfaces had no effect on DPF or the measured value for CBV. It
in the illuminated region.21 52 In adults, the optodes are was concluded that, provided the distance between light
generally placed on the forehead for reasons of accessibility entry and exit on the scalp is sufficiently large, changes in
and this represents the anterior cerebral circulation. How- scalp blood flow have no effect on NIRS measurements of
ever, in neonates it is obvious that most of the head is cerebral haemodynamics.
illuminated by the beam of light crossing it and the NIRS
signal is more representative of one or both hemispheres. Future developments
Much of the early work on quantification of haemo-
The principal problem affecting NIRS in adult medicine is
dynamic variables was carried out in neonates. As the non-
the effect of extracerebral tissue to scatter light and decrease
cerebral tissue of the head is so much thinner in preterm
the magnitude of the measurements. The contribution of
infants than in adults there are fewer problems with light
loss in the scalp and skull. For this reason the method of these layers is still unclear but the use of increasingly
CBF measurement described gives measured values for sophisticated computer modelling will permit a better under-
CBF which correspond with those simultaneously measured standing of these effects. Furthermore, with modern equip-
by 133xenon washout.4 63 Although the correlation is good ment it will be possible to make real-time correction of the
at low to normal values, there is a tendency for CBFNIRS scattering effects of extracerebral tissue.
to overestimate CBFXe at high flows.63 Furthermore, the It is obvious that the non-invasive nature of NIRS is its
coefficient of variability for CBFNIRS in both infants63 and main advantage. The equipment is also suitable for use at
adults14 is greater than for 133xenon. This means that it is the bedside, thereby avoiding the necessity to transfer
necessary to make several measurements in order to obtain critically ill patients to remote scanning suites. A third asset
a reliable mean value for CBF. However, the non-invasive is that no radionuclides are required. Finally, the data are
nature of NIRS compared with other methods of measuring provided on a real-time basis as often as twice a second.
CBF is an enormous advantage which may offset the greater The variety of data which can be measured by NIRS
variability. (real-time cerebral oxygenation and CBV changes, and
At present, NIRS methods in adults strikingly underesti- absolute CBV and CBF measurements) contributes to its
mate CBF54 and this is likely to relate to the contribution potential. An exciting new development is the application
of non-cerebral tissue overlying the cerebral tissue in the of NIRS in functional imaging. Changes in HbO2 concentra-
field of view. The head is not opaque to infrared light, but tion can be detected over the occipital cortex in adults in
scatters the light very intensely and computer modelling response to visual stimulation49 66 and over the frontal
has shown that in a typical volume of tissue interrogated cortex in response to calculation tasks.30
by NIRS, approximately 30% is brain and 70% is non- It is important that simple technical details such as optode
cerebral (i.e. scalp and skull).29 Although the DPF applies designs which reduce sensitivity to movement and the
to the entire illuminated tissue volume and its scattering effects of ambient light are appreciated, as commercial
properties, because extracerebral blood flow is low,22 only equipment is in a relatively early stage of development.
30% of the illuminated volume has a rapidly varying HbO2 The problem of changing source–detector separation during
concentration when SpO2 is altered during CBF and CBV the course of a measurement is also being addressed; if this
measurements. It is probably for this reason that NIRS- distance changes, the resulting changes in attenuation are
derived CBF and CBV in the adult subject have values not easy to differentiate from concentration changes. The
approximately 70% less than those predicted by other next generation of equipment will allow measurement of
techniques. This is confirmed by a study which showed total optical pathlength and compensation for the movements
that, whereas mean CBF was measured as 67 ml 100 which inevitably occur during clinical use.
g–1 min–1 when the optodes were placed directly on the NIRS techniques in adults remain only promising pos-
dura, the value was only 23 ml 100 g–1 min–1 when sibilities at present, but steady progress is being made in
measured transcranially in the same subjects.54 However, a their development. It is clear that a bedside monitor of
more recent study has demonstrated a value for CBV much cerebral well-being will be invaluable. Commercial pressure
closer to the expected range25 and the relationship between to produce a marketable NIRS monitor is intense but it is
transcranial NIRS measurements of CBV and CBF and the important that this pressure does not compromise the
values obtained using other methods is still far from clear. requirement to validate the use and reliability of NIRS
In an attempt to examine the contribution of scalp blood before its widespread release into clinical practice.
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