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268 V. Dini et al.
Daeschlein et al. 2017). Hyperspectral sensors (detectors) evaluate the reflectance
information of an object and provide reflectance spectra for each pixel in the image.
The data thus acquired can be used to reconstruct three-dimensional models. The
spatial resolution depends on the distance between the sensor and the measured
object. The acquired images are reprocessed using tabulated values for tissue
chromophores of interest (oxygenated and deoxygenated haemoglobin, melanin,
etc.) by estimating their concentrations (Xu et al. 2012).
This imaging method at wavelengths between 500 and 700 nm assesses the
concentration of oxyhaemoglobin and deoxyhaemoglobin in the tissue providing
maps of tissue O
level that allow for the assessment of wound healing potential
2
with use for example in diabetic foot and burn scars. These values were used to
predict diabetic feet at risk of ulceration, the potential to heal or the risk of the
development of chronic wounds (Nouvong et al. 2009). Compared with other
optical systems (such as earlier RGBs, laser-based systems or magnetic resonance
imaging), HSI has several advantages such as high achievable spatial resolution and
spectral resolution beyond the visible range.
This method, however, is not without disadvantages: the methods that acquire
the most data correspond to those with the highest cost, and numerous standardized
databases are needed for the proper acquisition of data in a standardized and
reproducible manner (Sen et al. 2016). Several studies have been conducted to
examine the potential appli cations of HSI for medical diagnosis of tissue condition
and for monitoring wound healing in clinical settings.
Yudovsky et al. in (2010) used HSI to detect and predict ulceration in the diabetic
foot concluding that this method can optimize wound care by predicting the risk of
ulceration and predicting healing outcomes (Yudovsky et al. 2010). Data on skin
oxygenation and perfusion can also be used to define the characteristics of irradiated
skin by providing prognostic data on skin reaction immediately after irradiation (Chin
et al. 2012). Calin et al. demonstrated in burn injuries how HSI can identify subcutaneous edema much more rapidly than laser Doppler scanning (Calin et al. 2015).
Khaodhiar et al. developed a healing index based on the measurement of
oxygen-haemoglobin and deoxyhaemoglobin at the wound site and in areas adjacent to the ulcer (Khaodhiar et al. 2007). They found significant differences
between tissue oxygenation of healed and unhealed foot ulcers. Spectrophotometric
analysis can also provide information about the layer of tissue that sustained the
injury, as hematomas near the surface have a different colour signature than those in
deeper tissues (Bohnert et al. 2000; Paul et al. 2015).
HSI has also been used to study ischemic wounds. However, because of its
limitations, it has not yet been widely proposed in clinical practice. Many HSI even
in this case the cheapest ones have poor reproducibility and low accuracy. We also
have inherent limitations due to the method. The acquired data are vulnerable to
variations in illumination, detection, and tissue surface conditions. Second, the
acquired data may depend on inter-patient variations in skin colour and adipose
tissue content. Clear correlations on tissue spectral properties and pathophysiological characteristics have not yet been made and adequate calibration tools are
lacking (Sen et al. 2016). Ultimately through the study of hyperspectral images it
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will be possible to better study tissue healing mechanisms by investigating other
chromophores such as mitochondrial cytochromes to establish cellular metabolism
and clustering of fibroblast populations. It can be possible to determine the spectral
signature of the cytochromes b/c, which are located on the membranes of mitochondria and involved in the ATP-synthesis (Wahabzada et al. 2017). Current
advances in sensors and machine learning technologies are also expected to provide
powerful new tools for human medicine.
Laser Doppler Imaging (LDI)
Laser Doppler perfusion imaging (LDI or LDPI) allows you to quantify microcirculatory flow in a well-de fined region of interest (ROI) of the skin. It is based on the
Doppler effect principle by analysing the changes in the wavelength of electromagnetic radiation reflected by erythrocytes moving in blood vessels. The magnitude and frequency distribution of the Doppler-shifted light are directly related to
the number density and velocity of blood cells. Tissue penetrating laser light
generates scattering and absorption with scattered light returning to tissue surface
being registered by a photo detector and calculated as blood flow in real time
(Kloppenberg et al. 2001).
Blood flow analysis can also be integrated with other classical imaging methods
such as digital photography has been applied to the assessment of burns, scars,
pressure ulcers, diabetic foot ulcers and venous leg ulcers. Providing prognostic
data on burn wound outcomes and healing times. Several studies have shown
greater accuracy in predicting the prognosis of various burn wounds than clinical
data alone (Bohnert et al. 2000). LDI was used to study the microcirculation of
diabetic wounds. pressure ulcers have also been studied using LDI. it has been
shown that in stage 1 pressure ulcers there is a difference in blood perfusion
between the skin areas of the pressure ulcers and the periwound undam aged skin.
By means of the combined methods of LDI and digital photography they were
monitored in the postoperative period.
LDI mainly is used in patients with burn wounds. The benefit of LDI consists of
an objective real time evaluation of burn wound depth but requires sophisticated
knowledge for evaluation and interpretation (Droog et al. 2001).
Laser Speckle Imaging (LSI)
Laser Speckle Contrast Imaging (LSCI or LSI) is a strictly qualitative laser-based
imaging technique used to study perfusion. Unlike the LDI technique described
above, this imaging technique is used to provide quality data on a larger surface. Its
principle of operation is based on the reflection of light waves by the moving blood
cells. When they are hit by photons, they generate some photons in phase and in
anti-phase (in a constructive and destructive way) that create shadow areas that
270 V. Dini et al.
change continuously. In contrast to stable particles objects in movement like red
cells in blood vessels show a speckle pattern changing over time in dependence of
the degree of movement which is recorded as blurring signal with a CCD camera.
In LSI, these randomly changing patterns are averaged over time to produce what is
referred to as “blur” which is related to blood flow. The advantage of this type of
acquisition is that it can be done quickly almost instantaneously. He Ne laser source
at 633 nm have been used on animal models and to study the performance of scars
(Paul et al. 2015).
Near-Infrared Spectroscopy (NIRS)
The operation of NIRS is based on the different degree of ligh t absorption in the
near-infrared spectrum of tissue components with different oxygenation states.
NIRS employs light emitting LEDs or laser diodes operating between 650 and 900
nm that illuminate the skin tissue, and the light is absorbed by various chromophores in the skin, particularly water, oxyhaemoglobin, and deoxyhaemoglobin.
Deoxyhaemoglobin has a maximum absorption at 760 nm, while oxyhaemoglobin
absorption is maximum at 900 nm. Water, useful for identification and quantization
of edema, has an absorption peak at about 980 nm contained in this range. The
reflected NIR light is collected by a detector and analysed to provide measurements
of chromophore content. Subsequent analysis of this data can be applied to the
assessment of wound severity and healing. NIR has potential use in wound
assessment because through it the degree of wound depth and quantification of
edema can be classified. The increased severity studied for burn wounds is
accompanied by decreased lesional vascularization.
Preclinical studies have shown that measurements of oxygen saturation and total
haemoglobin alone can differentiate a superficial burn wound from a full thickness
burn wound. This method has been seen to have a distinction between superficial,
intermediate partial-thickness, deep partial-thickness, and full-thickness wounds. In
detail, identifying a quantitative measure of water loss especially in the field of
burns is definitely a great potential for the use of NIR (Cross et al. 2009).
In diabetic wounds in animal models, it has been shown to differentiate diabetic
ulcers, based on reduced perfusion and greater tissue disorganization than in nondiabetic controls. NRI methods have also been used to analyse the process of
lesional neovascularization (Daeschlein et al. 2017).
Thermography
Due to the relationship between temperature and emissivity of infrared radiation (a
property intrinsic to all objects), thermography methods have been developed and
have found wide use in the field of dermatology and particularly wound imaging.
This correlation allows thermographic measurements of the skin to be analysed and
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Fig. 2 Thermographic image of a vascular ulcer of the right calf (lateral region)
processed to create color-coded images. This imaging method is known as IR
thermography or static IR thermography (Fig. 2).
Leveraging temperature recording by static thermography and thermal excitation
provided Dynamic active thermography (ADT) is an advanced thermographic
technique that involves recording steady-state temperatures using a standard IR
camera following thermal excitation of the tissue by a light source, usually halogen
lamps. A second set of temperature measurements is taken after thermal excitation,
and subsequent analysis allows quantification of the thermal diffusivity of tissue
components and wound regions (Renkielska et al. 2006).
Liquid crystal thermography (LCT) uses a plate of thermochromic liquid crystals
to measure tissue temperature distribution (Roback 2010; Benbow et al. 1994).
Liquid crystals absorb heat radiated from the tissue, and the plate emits a spectrum
of colours that correlates with temperature readings. The potential of thermography
as an aid in the evaluation of burn wounds was identified in the early 1960s by
Lawson (Lawson et al. 1961), who used infrared scanning to predict burn depth
with 90 percent accuracy, confirmed by histology. These predictions were based on
the simple principle that superficial burns may be warmer than healthy skin for the
inflammatory process, while deeper burns would be colder than healthy skin due to
structural damage done to vascularization.
Subsequent studies have been aimed at predicting the outcome of burn wound
healing, discriminating between wounds that heal spontaneously in three weeks or
272 V. Dini et al.
requires excision and grafting (Cole et al. 1990). A bias of the method lies in the
evaporation and loss of water from the wound bed especially that which occurs in
the early stages. By applying a nonpermeable cover to the wound bed (thus closing
off the system), the problem of evaporative cooling can be circumvented thermographic measurements to be taken even in the early stages. This expediency is
useful since burns are best assessed within 3 days because of the subsequent heating
of deeper burns (Liddington and Shakespeare 1996). Recent studies have used
high-resolution digital infrared cameras with increased specificity, distinguishing
between full-thickness, deep partial-thickness, and superficial partial-thickness
burns (Hardwicke et al. 2013; Medina-Preciado et al. 2013). Studies comparing
static thermography methods with dynamic methods have demonstrated the superiority of the latter in terms of accuracy, specificity, and sensitivity in determining
the degree of depth of burn wounds (Renkielska et al. 2006).
Thermographic devices are cheaper and easier to use than laser methods (LDI),
and are much more accurate than visual assessment, however, further studies are
needed. In the evaluation of the diabetic foot, it has been established that increased
temperature can be considered a reliable marker of inflammation by providing
predictive data on the risk of ulceration at the different sites explored and has also
been correlated with the risk of amputation and infection (Bharara et al. 2012).
In 1994, Benbow et al. found that mean foot temperature, determined from eight
standard sites on the plantar surface, could be used to assess the risk of ulceration
and ischemic foot disease (Benbow et al. 1994). Diabetic patients with high mean
foot temperature were at incre ased risk of neuropathic foot ulceration, while those
with normal or low mean foot temperature were at risk of ischemic foot disease.
Another method of temperature assessment is to perform an analysis of temperature
variation between feet of the same patient.
About pressure ulcers, slow-healing and normal-healing pressure ulcers were
identified by thermography in a 1973 study. This study showed that slow-healing
ulcers were characterized by a temperature of less than 1 °C compared with the
surrounding skin, whereas normal-healing ulcers had a temperature difference of
2.5 °C (Barton and Barton 1973). Newman and Davis studied patients admitted to a
geriatric unit and succeeded in providing an estimate of the risk of insurgence of
sacral pressure injuries (Newman and Davis 1981).
A higher temperature at the wound site than in the surrounding skin implies the
presence of factors that may inhibit wound healing providing an instrumental
finding that anticipates traditional clinical signs. With a view to preventing the risk
of press ure injury occurrence, thermographic imaging of pressure injuries has been
compared to the Braden Scale, the most common tool for predicting press ure
injuries.
Thermography has also been used to monitor wound healing of venous ulcer
aetiology (Judy et al. 2011; Mercer et al. 2008). In a study we recruited 18 patients
affected by venous insufficiency and lower leg ulcers. A total of 24 chronic wound
bed and perilesional skin ulcers were assessed using an infrared camera and from
this was showed a relationship between the wound bed score and the wound bed
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temperature according to several studies that have demonstrated 33 °C is the critical
temperature level required for normal cellular activity (Dini et al. 2015).
In portable thermography, including using devices such as smartphones and
tablets is gaining momentum and will bring major changes not least in terms of
costs of devices.
However, this method, which is gaining momentum with promising results, is
not without its difficulties. The main limitations are due to technical difficulties such
as proper positioning of the patient and acquisition instrumentation and lack of
correlations with validated quantitative scales (Paul et al. 2015).
Videomicroscopy
Videomicroscopy captures photons from a fibre optic light source through a
magnifying glass, enabling direct skin micro-imaging. It has a certain degree of
invasiveness as it requires direct skin contact. Advances in microscopy allow for
visualization of skin tissue at the cellular level and can be used for non-invasive
histological analyses. Traditionally, the use of light microscopy in conjunction with
histological analysis is the gold standard for determining burn wound depth. Since
the relationship between skin capillary plexus integrity and burn depth has been
established, videomicroscopy provides the information needed to determine burn
depth with accuracy comparable to LDI and clinical evaluation. It measures
directly, without artifacts caused by histological sampling, the microstructures of
great importance in the study of wound and periwound micro-vascularization.
McGill et al. claim that the advantages of videomicroscopy over LDI are easier
portability, reduced cost, non-variation due to patient movement, skin curvature or
ambient light. In videomicroscopy there is little chance for the patient to have
discomfort or infection but is instead a very well tolerated method. There are still
numerous studies that validate it (McGill et al. 2007).
Optical Coherence Tomography
OCT generates high-resolution images of tissue microstructure in 2D images by
exploiting low-coherence interferometry which works by optical scattering from
tissues that measures the echo delay of these waves. A laser light beam is split into
two separate paths: one is focused into the tissue and the other is guided into a
reference point. The reflected light beams from both targets are recombined to
generate an interference pattern (Paul et al. 2015). The reflections obtained from the
target area are correl ated with the reference light with distinct tissue propagation,
thus enabling structural information of even larger tissue areas to be obtained. OCT
systems do not require contact between probe and skin making the method minimally invasive (Li et al. 2020). The field of application of OCT in skin wounds lies
more in monitoring structural changes by allowing quantification of newly formed
skin tissues.
274 V. Dini et al.
A variant of OCT that takes advantage of the bi-refringence characteristics of
tissue elements (e.g., collagen) is polarization-sensitive OCT (PS-OCT), using a
polarizer we can determine the depth of lesions with an accuracy comparable to
histological analysis (Srinivas et al. 2004). This assessment is achieved by correlating burn depth OCT is further improved for burn imaging by an extension of
PS-OCT, Mueller matrix OCT (Todorović et al. 2008). Jiao et al. demonstrated that
Mueller matrix OCT, which separates phase-based from amplitude-based polarization contr ast, can collect more detailed information from tissues, which is also
applicable to burn depth assessment (Jiao et al. 2003). OCT angiog raphy has been
used to quantify wound area and rate of wound contraction.
Using PS-OCT, an analysis of the micro-vascularization of burn wounds can
also be performed. Kim et al. used a combination of microvascular measurements
and birefringence data to characterize burn depth claiming that PS-OCT can allow
more immediate and cost-effective detection than current standards (Kim et al.
2012). Data obtained from OCT can be used clinically to monitor scar progression
after a burn (Liew et al. 2013). Ultra-high-resolution OCT allows identification of
wound size, epidermal migration, dermal-epidermal junction formation, and wound
composition, lending itself as a detailed and non-invasive metric of wound healing.
OCT can be used to monitor wound re-epithelialization, as it accurately differentiates epidermal and dermal layers. In addition, measurements of wound size,
inflammation, re-epithelialization, and early resorption aid in monitoring assisted
wound healing. OCT may also prove to be a useful tool for the study of chronic
wounds, where epidermal and dermal structure may be compromised, and
re-epithelialization is problematic. Quantitative data on epithelialization, collagen
deposition, and inflammation can be obtained noninvasively with accuracy comparable to histology, which is preferable to invasive biopsies that may interfere with
the healing processes being studied.
Dynamic “OCT (D-OCT)” is a new methodology to visualize the skin vasculature through motion detection from speckle variance (Mariampillai et al. 2008;
Themstrup et al. 2016). Initial imaging of blood vessels in burns and wounds is
promising; the development of D-OCT allows visualization of capillaries up to 20
lm in diameter and perfusion of the mid/upper dermis, which could allow understanding of the contribution of blood substances to wounds (Schuh et al. 2017).
This offers potential advantages over photoplethysmographic techniques that detect
changes in venous volumes in deeper tissues but without interpreting capillary
function.
D-OCT has been extended to the examination of perilesional skin. Since 2015,
software-based methods have been developed to detect blood flow from OCT
images by detecting microscopic changes between OCT images acquired in a very
short time interval
D-OCT is significantly different from Doppler-OCT because it uses intensity
changes rather to detect motion. Although Doppler-OCT has been shown to be able
to detect blood flow in the skin, it loses sensitivity due to high background noise
and because most of the blood flow is perpendicular to the laser beam (Zhao et al.
2000; Ren et al. 2002). D-OCT has the additional capability of being able to assess
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with sufficient resolution the size and morphology of blood capillaries even at depth
(Boas and Dunn 2010). D-OCT detects blood motion, on the order of 0.1 to 1.0
mm/s. Therefore, it filters blood vessels where blood is stationary or flows very
slowly or in lymphatic vessels.
Holmes et al used D-OCT, to study capillaries in periwound skin in 11 patients
with chronic wounds (of venous or arteriovenous etiology) of long duration.
Specifically, in a non-invasive way, they studied capillaries at the 4 poles along the
wound edge, the center of the wound, the skin proximal to the wounds placed at a
fixed distance and at a control site. In their study, they provi ded the anatomical and
functional characteristics of the explored sites providing useful clinical-instrumental
information to enable more scientific advances in this promising wound imaging
method (Holmes et al. 2019).
Fluorescence Imaging
Fluorescence imaging (FLIM) takes advantage of the endogenous fluorescence
emitted by the skin's natural fluorophores (such as collagen and elastin) and can
complement the fluorescence analysis of exogenous fluorescent materials. The skin
is irradiated by a laser source with specific excitation wavelengths and captures and
filters the light at the wavelength of interest. Injection into the bloodstream of
indocyanine was used as exogenous fluorescence and its fluorescence levels correlated with vascularity and burn wound depth (Still et al. 2001).
In FLIM, on the other hand, the fluorescence of, nicotinam ide adenine dinucleotide (NADH) in the wound bed is measured. NADH is involved in oxidative
phosphorylation and signals c ellular metabolism that can be used as a marker for
skin wound healing. The main drawback of this technique is that it requires a dye
injection to provide blood flow measurements.
FLIM and Second Harmonic Imaging (SHG) were combined and used in the
study of wound healing. Through FLIM, cell metabolism rates can be monitored by
measuring NADH levels while SHG can assess collagen deposition at the wound
bed site. These methods taken together are comparable to histochemical analysis
and may be suitable for the study of skin wound healing (Deka et al. 2013). FLIM
correlating with cellular metabolism can prove to be a useful marker of tissue
vitality in the study of the healing process in skin wounds (Queen and Harding
2020). Devices that assess the fluorescence of endogenous bacterial porphyrins
noninvasively and in real-time have also been devised.
Gram-positive emit a red fluorescence, while pyoverdine of Pseudom onas
aeruginosa and other Gram-negative bacteria emit a cyan fluorescence.
Light green fluorescence corresponds to slough, dark green fluorescence to
granulation tissue, black color for necrotic tissue and dark red-purple-black for
vascularized areas (Janowska et al. 2021). Le et al. used this technology on 350
patients. They found that 82% had bacterial loads >104 CFU/g with failure to detect
infection in 85% of cases using Clinical Signs and Symptoms Checklist (CSSC)
assessment alone (Le et al. 2021). In a retrospective study of 229 foot ulcers,
276 V. Dini et al.
fluorescence imaging was correlated with a 49% reduction of antimicrobial dressings, a 33% in systemic antibiotic, and a 23% increase in wound healing rate (Price
2020).
In a study, a handheld autofluorescence device was used to evaluate the
reduction of bacterial load associated with 3 different therapeutic approaches by
correlating images acquired with NRS pain scale, Wound Bed Score (WBS), and
quality of life (QoL) assessment demonstrating a superiority of zinc oxide bandage
over dressings and multic omponent bandages or sharp debridement, dressings, and
multicomponent bandages (Janowska et al. 2022).
Confocal Microscopy
Confocal microscopy or confocal laser scanning microscopy (CLSM) has recently
become commonly used in the field of dermatology. It is a high-resolution optical
detection technique using a light source and lens that allows images to be acquired
at multiple depth levels. A detector array collects re-emitted signals from the focal
plane, eliminating all backscattered photons from the surrounding material that
would appear blurred. The greatest advantage of this technique is based on the
ability to evaluate the skin in vivo by applying a kind of real-time cyto-histology.
It can in fact provide such detailed images that clear images of cells in the
epidermal layers’ be discerned, and at the dermal level it is possible to distinguish
cellular blood populations from the profile. Skin appendages such as sebaceous
glands, hair shafts and sweat-gland ducts can also be seen.
To cover the entire sample, manual scanning of the sample is always performed,
but because only a small region is illuminated at each acquisition step, confocal
microscopy is not ideal for large fields of view, although modern instruments have
been developed to cover larger areas. The quality of images obtained by CM can
depend on the technology used and the ability of the operator.
By changing the focal depth, this technique acquires a series of horizontal
section images, which can be reproc essed to provide a final image. CLSM can be
used to collect high-resolution images in different spatial planes at each stage of the
skin wound repair process. Because of its very high resolution, it can provide
information on histologic cellular and architectural morphology. With this technique, blood flow, new tissue formation, and tissue remodelling can be visualized
completely noninvasively (Paul et al. 2015).
At present, confocal microscopic technology is under continuous development in
almost all fields of dermatology. However, because of its excessive cost, the use of
confocal microscopy is for now only confined to research centres. With the
miniaturization of devices and the containment of costs it proves to be of immense
contribution in wound healing. it is one of the most promising methods.
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Ultrasound
Ultrasound (US) imaging, since its first use in 1979, It has been widely used and has
become more is very important in dermatology for a wide range of purposes, from
skin lesion localization and classification to pre- and post-treatment evaluation,
outcome assessment, and follow-up studies (Firooz et al. 2017; Kavros and
Coronado 2018). US is a versatile, painless, low-risk, and non-invasive procedure
that can be easily and repeatedly performed (Bhatta et al. 2018).
The most used probes in dermatology range from less than 10 MHz (traditional
US), 10–30 MHz (HFUS: High-Frequency US) and 30-100MHz (UHFUS:
Ultra-High Frequencies US), the choice depends on the clinical query (higher US
frequencies have better image resolution but limited depth of penetration compared
to lower frequencies). Another advantage that US allows is the ability to assess the
degree of vascularity through Doppler US evaluation.
Conventional US (frequency <10 MHz) and Doppler US evaluation are frequently used as an aid in diagnostic and therapeutic algorithms of chronic lower
extremity, in order to evalua te the nature of the lesions and identify the presence of
alterations in the venous and superficial circulation (Izzetti et al. 2021; Kirsner and
Vivas 2015). US have also been used to study the depth of wounds and define the
involvement of various skin structures (Flanagan 2003). When evaluating a skin
wound with US, it is recommended that highly trained personnel is recruited,
because this technology is operator dependent (Mani et al. 2016).
HFUS is used for wound healing from 1990. HFUS has been used to evaluate
the efficiency of therapeuti c intervention on healing scars (Kerckhove et al. 2003).
Hoffman K. et al have described by means of the HFUS the phases of healing of a
cutaneous wound comparing through the follow-up of cryotherapy wounds but the
differentiation between necrotic tissue, fibrous tissue, neo-epithelium, and granulation tissue was very difficult (Hoffmann et al. 1993).
Tissue analysis by HFUS has been proposed as an aid method in the prevention
of pressure injuries in bedridden patients (Dyson et al. 2003). The potential of
HFUS in wound monitoring with a wound dressing in situ was proposed (Ke nney
and Delves 1997).
The use of UHFUS in the study of ulcerated lesions has shown encouraging
results. UHFUS modern machinery can provide ima ges with resolution in the
30-micron range (Izzetti et al. 2020a, b; Oranges et al. 2019). For its higher resolution UHFUS can provide establish an estimated amount of granulation tissue,
depth of necrotic tissue, physical dimensions of the wound, wound volumes and
structural components (Fig. 3)
UHFUS could also quantify the degree of edema of the lower limbs, providing
objective parameters on its decrease according to the type of bandage.
The new machines for skin ultrasound can also provide in a single frame an
entire scan of the surface of the lesion. By means of the software often supplied
with the machines it is also possible to reconstruct the ultrasound structure in 3D
post acquisition providing a wound growth tracking US not only in 2D.
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