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10.6.1 Photothermal therapy (PTT)
PTT is an effective and non-invasive therapeutic treatment of cancer. It is a particular
type of hyperthermia in which body tissues are exposed to higher temperatures to
induce the elimination of abnormal cells. Light energy produced from laser is used to
produce localized heat which causes heat ablation of tumour cell [66]. In PTT, the targeted abnormal cells are l abelled with photoabsorbent nanoscale particles (also
named as photothermal agent (PTA) or photosensitizing agent) [67]. Activation of PTA
is done by pulsed near-infrared (NIR) laser light. The use of PTA boosts the light absorption by targeted malignant cell without damaging the surrounding healthy tissues
and increases the penetration of NIR laser light. Absorption of light by the photosensitizing agent increases the temperature and causes local hyperthermia, which results
in thermal ablation of the targeted tumour cell [68].
For developing an effective PTT strategy, an ideal PTA should have good biocompatibility, large absorption cross section, and high photothermal conversion efficiency
(in transparent NIR window of 700–1,100 nm) along with the ease in functionalization.
PTT has an advantage over conventional therapeutic treatments (like chemotherapy
and radiotherapy) as biocompatible nano-sized particles (PTA) cause less side effects
and selective thermal destruction of cancerous cell present deep in the tissue. PTT can
be coupled with chemotherapy to improve therapeutic effectiveness [69].
There are three operating modes of PTT: (a) light only, (b) light with endogenous
substances, and (c) light with exogenous substances. The third option is the most operative for heat generation due to metal’s high photothermal conversion efficiency. It
should be highlighted, however, that using nanoparticles (NPs) as enhancing PTT agents
raises concerns regarding their targeted delivery as well as side effects of metallic nanostructures and potential cytotoxicity. Metal nanostructures can be targeted and delivered to the specific cancer tissues using mechanisms such as antibody–antigen or
ligand–receptor interaction. Noble metals like silver and gold are less toxic and biocompatible, making them ideal for PTT applications [70].
10.6.2 Mechanism of heat generation in photothermal therapy
Laser light interaction with tissue generates heat, which is the major principle of heat
generation mechanism in PTT. Microscopic and macroscopic level studies can be performed to determine the interaction between laser light and tissue. Laser contains energy in the form of high-frequency electromagnetic waves which on interaction with
tissue gets converted to heat energy [71]. According to the macroscopic model, heat generation is linked by the penetration of laser light into tissue during laser–tissue interaction. When tissue is irradiated with laser, few beams are reflected and rest of them
penetrate deeply into the tissue. The light that gets through is susceptible to absorption
and scattering. The absorption coefficient is defined as the loss of incident radiation
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with depth. The scattering coefficient is characterized as the loss of laser energy due to
scattering per penetration length unit. These two coefficients are tissue specific and laser
wavelength dependent. Beer’s law describes the beam attenuation in the case of laser
light. To begin, consider an absorber rather than a scattering sample. Beer’slawdescribes
the beam attenuation according to which the heat generated in tissue is dependent on
the absorbed energy. Commonly, the light falling on the sample is simultaneously absorbed and scattered. Beer’s law still applies to this beam attenuation. The attenuation
coefficient, also referred to as the total attenuation coefficient, is the sum of absorption
and scattering coefficients [72].
In case of microscopic model, excitation of the molecule occurs from normal to excited state when energy in the form of photons hits a molecule, as shown in Figure 10.3
[73]. By the neighbouring M1 (a molecule, an atom, or an electron), the excited molecule
experiences an inelastic collision, which transfers some of its energy and causes it to
decay into a stable state molecule. Due to microscopic increase in temperature, thermal
vibration of M1 molecule also increases. The concentrated M-type molecules absorb energy from large photon flux by laser beam, and this energy is converted to thermal vibration, and heat is responsible for temperature increase.
Figure 10.3: Representation of mechanism involved in photothermal therapy (Lasers in Medical Science
2008:23 217–228, originally published by and used with permission from Springer Nature).
Both necrosis and apoptosis are common causes of cell death in PTT. Necrosis is defined
as the uncontrolled cell death due to interior and exterior pressures such as chemical
pathogens or mechanistic injuries. This results in breakdown of plasma lemma integrity
and subsequent leakage of protoplasm. Necrosisisanundesirablenaturalprocessofcell
death as aberrant release can cause harmful inflammatory and immunogenic responses
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[74]. Apoptosis is a programmed cell death when cells preserve their membrane integrity
by phagocytosis and prevent inflammation. Apoptosis can result in secondary necrosis,
causing losses to the cell membrane integrity and releases damage-associated molecular
patterns but does not activate the engulfment process [75]. To date, necrosis has been
described as the common in vitro immune response to phototherapy; however, few studies indicate apoptosis as the main mechanism of cell death by light exposure [76].
If no external agent is utilized, the PTT process is unable to distinguish between
normal and malig nant cells, thus causing damage to both. Superficial healthy tissue
will be subject to more damage because of more light exposure (i.e. larger energy) as
compared to diseased tissue present deep inside. It is important to mark tumour cells
with NPs carrying light absorption agents to vary the response of tumour cell by increasing its energy absorption for selective photothermal treatment. The use of NPs
enables the variety of unique features and speci fic heat responses from body cells.
Due to enhanced permeability and retention effect, nanomaterials in PTT are injected
either intravenously or intratumorally [77].
The conduction-band electrons in NPs create synchronized oscillation which generates heat when tumour is exposed to light at resonant energy. This heat can bring
permanent cellular harm and reduction in tumour size by increasing the temperature. The rise in temperature of this tumour depends upon three factors: the amount
of delivered light, NP concentration in tumour, and photothermal conversion efficiency of NPs. NPs which can absorb NIR light of wavelen gths (650– 1,064 nm) have
greater chances to cause thermal ablation. This specific wavelength range can deeply
penetrate to biological tissues than v isible wavelength due to its minimum absorption by haemoglobin and water [ 78].
10.7 Carbon dots in photothermal therapy
CDs act as PTAs due to the following reasons: (a) photothermal conversion efficiency, (b)
rich in π-electrons, and (c) substantial temperature variations when irradiated [79]. In
recent years, CDs have been used as photosensitizing agents like red-emissive CDs (RCDs), which show red emission, low cytotoxicity, good QY (22.9%), photothermal efficiency (43.9%), and two-photon excited fluorescence (Figure 10.4). The R-CDs can convert
laser energy to heat energy very quickly upon irradiating for 10 min with laser. When
the concentration of R-CDs increases by 20–200 μg/mL, the growth of MCF-7 cells is sig-
nificantly reduced [80].
Geng et al. prepared N-O-CDs (nitrogen- and oxygen-doped) which are irradiated by
laser of low power density. It causes 100% reduction of tumour with minimum side effects. The prepared N-O-CDs show photostability and biocompatibility, and has strong
NIR absorbance [81]. S- and Se-co-doped CDs were prepared by using diphenyl diselenide and polythiophene as source of carbon. The doping enhances photothermal
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Figure 10.4: Red-emissive CDs and their applications (Carbon 2020:162,220–233, originally published by
and used with permission from Elsevier Ltd.).
conversion efficiency to 58.2%, making applicable as multidimensional phototheranostic
agent for cancer treatment [82].
Wang et al. prepared nitrogen- and boron-doped CDs (N-B-CDs) showing NIR absorption (1,000 nm) to enhance deep tissue penetration. The conversion of NIR to heat
by N-B-CDs exhibits photothermal therap eutic effect by inhibiting tumour growth and
killing cancer cells. N-B -GQDs exhibit safe profile, rapid excretion in mice, and prolonged half-life in blood, which make them compatible for biomedical applications
[47]. In another study, iron-doped CDs (F e-CDs) with size of ~ 3 nm are synthesized,
which exhibit effective photo-enhanced enzyme-like characteristics and photothermal
conversion. Fe-CDs act as PTA and nanozyme that exhibits antibacterial ratio against
E. coli and S. aureus. This study shows the wound h ealing efficacy of Fe-CDs by increasing fibroblast proliferation and angiogenesis, and preventing infection and collagen deposition [83].
CDs with photosta bilit y, controlled size, and low biotoxic ity are excellent contrast agents for optical imaging. Mostly, CDs activated by ultraviolet light exhibit visible/NIR emissions of less than 820 nm, hence, reducing bioimaging applications due
to low penetration depth. It is necessary to synthesize photothermal-based CDs with
NIR-II emission I in the range of 1,000–1,700 nm. Li et al. hydrothermally prepared
NIR-II-emissive CDs from watermelon which possessed biocompatibility, photother mal conversi on efficienc y, photostability, QY, and renal clearance [84], as depicted in
Figure 10.5.
In another study, sulphur- and nitrogen-co-doped NIRCDs were prepared via solvothermal method from citric acid, dimethyl sulphoxide, and urea as precursors for
carbon, nitrogen, and sulphur, respectively. The prepared S,N-CDs exhibit excellence
in photo-caust ic imaging, photoluminescence imaging and in PTT [85]. Permatasari
et al. prepared p yrrolic-N-r ich CDs derived from concentrated urea by microwaveassisted hydrothermal method. These N-CDs have first NIR absorption peak at 650 nm
and have negative charge on surface. They act as multifunctional carriers in cell imaging, targeted drug delivery, and PTT [86].
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Figure 10.5: Synthesis mechanism of NIR-II-emissive CDs from watermelon (Bioactive Material
2022:12,246–256, originally published by and used with permission from Elsevier Ltd.).
Zhang et al. designed an approach by combining PDT and PTT. In their study, a nano-
structure has been developed from the hybrid mixture of iron oxide CDs (Fe
-CDs) and
3O4
phosphorene quantum dots (BPQDs) known as genipin [GP]-polyglutamic acid [PGA]-
-CDs@BPQDs, as shown in Figure 10.6. This nanostructure has biocompat ibility
Fe
3O4
and photodegradability, and exhibits sturdy light absorption band [87].
Figure 10.6: Preparation mechanism of GP-PGA-Fe3O4-CD@BPQD nanocomposite (International Journal of
Nanomedicine 2018:13 2803–2819, originally published by and used with permission from Dove Medical
Express Ltd.).
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Huang et al. hydrothermally formulated S-, Se-CDs (sulphur, selenium co-doped
CDs) with good fluorescence QY. T hese nanostructures have antioxidant property
due to SH and Se-SH groups which enhance the reactive oxygen species scavenging
[88]. Peng et al. introduced simple, ecological, and economic m ethod to synthesize
CDs decorated with Prussian blue dye ( CDs@PBNP). The nanocomposite has combined character istics of CDs such as biocompatibility, photoluminescence, and photothermal conversion ability of Prussian blue [89]. Knowing the importance of CDs
as photothermal agents, a comprehensive view of different materials reported is
given in Table 10.2 with photothermal efficiency, quantum yield and applications.
Table 10.2: CDs acting as photothermal agent, photothermal efficiency, quantum yield, and applications.
Photothermal therapy
(PTT) agents
NIR–II–CDs ~.% -N/A- Tumor treatment []
Red-emissive CDs (R-CDs) .%(.%) Nucleolus imaging, cancer therapy
N-O-CDs .% .% Cancer therapy []
S-, Se-co-doped CDs ~.%~.% Photothermal therapy of cancer []
Near-IR fluorescent CyCD .% .% Cancer imaging and therapy []
Fe-CDs .% -N/A- Wound healing and antibiotic therapy []
NIR-II CDs .% .% Bioimaging and photothermal
S-, N-CDs % -N/A- Biomedical applications []
Pyrrolic-N-rich CDs .% -N/A- Bioimaging, drug delivery, and
Photothermal
efficiency
Quantum
yield (QL)
Applications Ref
[]
and drug carrier
[]
therapy of cancer
[]
photothermal therapy
10.8 Clinical challenges of CD-based
photothermal therapy
CD-based materials designed for PTT have gained growth, but smart CDs of clinical value
remain in infancy. CDs hold the potential but there are clinical challenges that hinder
their applications. Focused efforts are required to implement cost-effective, low-toxic, and
biocompatible carbon nanomaterials such as PTT solutions in biomedical applications.
The challenges focused on commercial and clinical aspects of PTT based on CDs are
discussed:
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i. CD nanomaterials should be developed via simple and low-cost approaches, in-
cluding the diversity of mass production at industrial scale. Issues such as controlling size, batch-to-batch reproducibility, and purification must be considered
for large-scale synthesis.
ii. The development of multifunctional CDs will endure expansion of CD-related bio-
medical significance. This can be perceived by designing new precursors as carbon sources with properties like strong emission in NIR-I (700–900 nm) or NIR-II
(1,100–1,600 nm) with high QY and multimodal bio-imaging functions in combination with imaging technologies such as MRI and CT. Such hyphenation will extend
the application of CDs for cardiovascular, cerebrovascular, and respiratory system diseases.
iii. Introduction of CD assemblies with improved hydrophobicity or hydrophilicity
and light response in NIR region is vital. Such self-assembled CDs system can remove limitations as short circulation time in blood, in vivo instability, and relatively low tumor-homing ability.
iv. PTT with CDs must focus on incre asing the ef ficacy, accur acy, and safety of the
treatment. This demands systematic and detailed studies for exploration of their
biological effec ts as biodistribution, metabolism, biodegradation, and prolonged
toxicology and secretion of CDs.
These challenges require concern from researchers and clinicians to translate current
CD nanomaterials from the bench to the bedside.
10.9 Conclusion
CD development has offered practical approaches in PTT. It is believed that advancements in potential CDs will contribute to PTT; however, challenges will continue to hinder
the clinical applications. The research in nanotechnology is required to develop CD-based
PTAs to overcome the hurdles in cancer treatments. The preliminary works reported for
CDs with functionalized surface and various synthetic approaches are promising because
of their properties such as small size, functionalization potential, and the ability to be applied as PTA. The enhanced photoluminescence of CDs can have an advantage in treating
cancer. Combining the therapeutic functionality with improved cancer treatment can address the challenges of PTT. CD-based nanomaterialsasPTAarestillinthedevelopment
phase. They hold the technical capability to develop future therapeutics of targeted and
complete cancer treatment.
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