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412 N. Nomikou et al.
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in a site-specific manner has also been developed with applications in the treatment
of cardiovascular disease (Chorny et al. 2010).
Instead of polymers, gold can be used as a shell for the magnetite nanoparticles,
based on its biocompatibility and capacity to chemically bind a variety of molecules
(Fig.
15.10b). One characteristic example is the system composed of gold-coated
nanoparticles loaded with doxorubicin, the amine group of which binds to the
Fe
3O4
gold shell (Kayal and Ramanujan 2010). A novel approach has been designed for an
innovative application called directed enzyme prodrug therapy (Gwenin et al. 2011).
This approac h involves conjugating a genetically modified prodrug-activating
enzyme onto the surface of gold-coated Fe
nanoparticles. The direction of the
3O4
enzyme-carrying nanoparticles to the target site using a magnetic field can afford
activation of the prodrug at the site of the disease. A system with an alternative to
polymer or gold coating ha s been developed for theranostic applications in cancer,
and it is described as a mesoporous nanostructure with both upconversion luminescence and magnetic properties, consisting of a SiO
by rare-earth-doped NaYF
shell and carrying doxorubicin (Zhang et al. 2012). The
4
-coated Fe3O4 core surrounded
2
system significantly improved doxorubicin targeting in murine tumours in the
presence of an applied magnetic field.
One of the major attributes of magnetic nanoparticle-based systems is the
multifunctionality that they can offer. Magnetic guidance for targeted drug delivery
can be combined with magnetic hyperthermia for either hyperthermic ablation or
controlled drug release, as well as with imaging, since the nanoparticles can serve as
a contrast agent for magnetic resonance imaging (MRI), in vivo. Hence, these
systems are most commonly developed as theranostics. Core-shell type
nanoparticles, consisting of superparamagnetic iron oxide nanopar ticles (SPIONs)
coated with mesoporous silica and/or lipid and carrying doxorubicin have been
developed for theranostic applications in drug delivery, magnetic hyperthermia,
and as contrast agents (Patil-Sen et al. 2020). The nanoplatforms in this study
enhanced the quality of MRI imaging, induced ablative hyperthermia upon the
application of an oscillating magnetic field, and served as doxorubicin carriers.
However, the design of the nanostructures described in the study afforded only
passive release of doxorubicin, at 37 °C, as distinct from magnetic field-triggered
release. The use of thermosensitive polymers (e.g. crosslinked PNIPAM hydrogels)
or lipids with reachable phase transition temperatures for carrying the chemotherapeutic agent can equip such magnetically responsive systems with the additional
attribute of on-demand hypert hermia-induced drug release (Satarkar and Zach Hilt
2008; Veloso et al. 2021). Importantly, the release rate of the entrapped therapeutic
agent can be controlled by the duration, intensity, and/or pulse mode of the applied
magnetic field.
A promising category of magnetic nanoparticles with a wide range of applications
in theranostics is the magnetoliposomes or magnetoresponsive hybrid liposomes
15.10c). These are liposomes carrying magnetic nanoparticles, which can be
(Fig.
incorporated in the hydrophilic core as a single nanoparticle or nanoparticle cluster
(Rodrigues et al. 2016; Calle et al. 2015), imbedded in the lipid bilayer (Choi et al.
2019; Shirmardi Shaghasemi et al. 2017), or conjugated on the surface of the
15 Stimulus-Responsive Nanoparticles for Drug Delivery 413
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liposomal membrane (Acharya and Chikan 2020; Ma et al. 2021). The latter
approach allows to make the entire liposomal core available for drug loading,
improving loading efficiency. The magnetic behaviour of magnetoliposomes
strongly depends on the size of the embedded magnetic nanoparticles and the
functionalization of liposomes with magnetic nanoparticles larger than 5 nm in
diameter with high efficiency is of considerable interest. Incorporating magnetic
pos
nanoparticles of sizes larger than 3.4 nm in the lipid bilayer of li
chall
is a major
enge, and for this reason, multiple studies have focused on develop-
omes, however,
ing methods to make this possible, including for magnetic particles as large as 15 nm
(Choi et al.
2019).
Based on current progress, magnetic guidance for achieving spatial control in
drug delivery is a concept that has not been adequately explored and optimi zed for
clinical translation. Most published studies in this context describe innovative
systems that have only been tested in vitro, using either cell-free or cell-based
experimentation. Some studies have provided stronger proof of concept results,
exploring the translational potential of such systems by means of in vivo experimentation, mainly in small rodents. Despite the positive outcomes in these early in vivo
studies, magnetic guidance is achieved by simply placing a strong magnet against a
superficial tumour or defective site, a setting that would not be feasible for the
treatment of deep-seated tumours or diseased sites in clinical applications. Essentially, extensive and strategic preclinical in vivo and/or early-phase clinical investigation needs to be completed to verify the clinical feasibility of the magnetic
targeting concept, mainly with respect to the biodistribution and bioavailability of
the drug-carrying magnetic nanoparticles, their long-term safety after repeated
treatments, as well as a variety of critical aspects related to the externally applied
magnetic field, such as the required technological platform and the exposure parameters, in order to achieve site-specific nanoparticle accumulation, in a minimally
invasive manner.
An important matter for consideration is also the extent of spatial guidance or
targeted accumulation afforded with the application of an externally applied magnetic field. Non-specific accumulation in healthy organs and tissues remains an issue,
since magnetite causes oxidative stress disrupting normal cellular function, as well
as inflammation and neurobehavioral alterations in animal models. The polymeric
and other coatings used for rendering these nanosystems biocompatible are biodegradable and, moreover, they can be removed in the acidic endolysosomal conditions upon cellular uptake, exposing the reactive surface of Fe
3O4
.
15.3.4 Ultrasound-Responsive Nanoparticles
Ultrasound is among the safest and most promising stimuli for the spatiotemporal
control of drug release, since it is not associated with ionizing radiation, it can be
applied in a non-invasive manner, and it can be transmitted efficiently through tissue
allowing locoregional drug release even in deep-seated sites. The frequency of
414 N. Nomikou et al.
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Fig. 15.11 (a) A nanoemulsion droplet forming microbubble upon ultrasound exposure, (b)
Non-inertial and inertial cavitation under an ultrasonic field
ultrasound can be adjusted to optimize exposure at different depths in the body.
More specifically, for targeting superficial lesions/defects, an ultrasound frequency
at 5 MHz is normally employed, while frequencies 0.5–1 MHz are used for the
treatment of deep-seated regions or when transmission of ultrasound to the target is
impeded by attenuating structures, such as the skull. The acoustic energy deposited
adjust
at the target site for activating drug release can be tuned by
intensity and
duty cycle. The formulations that have been developed as ultrasound-
ing the ultrasound
responsive nanocarriers are nanobubbles, liquid perfluorocarbon droplets, MSNs,
and micelles/liposomes. These nanocarriers exploit the ultrasound-induced mechanical effects, such as cavitation, or the high-intensity ultrasound-induced heating
effect for on-demand drug release in a site-specific manner.
Perfluorocarbon (PFC) nanoemulsions offer an efficient system for low-intensity
ultrasound-mediated drug delivery (Zhong et al. 2019). They can serve as carriers of
hydrophobic drugs and can accumulate in tumour tissues via the EPR effect. PCF
nanoemulsions offer the attribute of forming microbubbles through acoustic droplet
vaporization under an ultrasonic field (Fig. 15.11a). When the formed microbubbles
are further exposed to ultrasound, they are forced to oscillate in size or shape, a
phenomenon called non-inertial cavitation (Fig.
15.11b). When microbubble diam-
eter during non-inertial cavitation grows to at least twice its original diameter, it
violently collapses and fragments to smaller bubbles, a phenomenon called inertial
cavitation (Fig.
15.11b), with subsequent drug release. Both non-inertial and inertial
cavitation cause microstreaming, which can generate transient pores on membranes
of cells that are in close proximity increasing their permeability. Essentially, when
the formed microbubbles are subjected to cavitation, they can promote cellular
uptake and/or release of the entrapped drugs in a site-specific manner. Similarly,
drug-containing echogenic liposomes enclose nanoemulsions (Fig. 15.12a), pockets
15 Stimulus-Responsive Nanoparticles for Drug Delivery 415
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Fig. 15.12 (a) Ultrasound-responsive liposomes, containing a. nanoemulsion in the core, and (b)
pocket of air in the shell
of air (Fig. 15.12b), or nanobubbles within their core and can respond to an
ultrasonic field facilitating drug release and cellular uptake (Huang and MacDonald
2004; Kopechek et al. 2008; Batchelor et al. 2020; Ezekiel et al. 2021).
The responsiveness of MSNs to ultrasound makes them a suitable drug carrier for
on-demand drug release using low-intensity ultrasound. The hydrophobic internal
channels/cavities of these porous nanosystems can accommodate hydrophobic
drugs, such as paclitaxel, as well as store gas in the form of nanobubbles, with the
nanosystems promoting drug release upon exposure to an ultrasonic field, in a sitespecific manner (Wang et al. 2018; Ho et al. 2020). More recently, metal–organic
frameworks (MOFs) have gained significant attention as drug nanocarriers due to
their advantageous physicochemical properties, including their responsiveness to
low-intensity ultrasound. The release of chemotherapeutic agents accommodated in
the porous structure of these nanocarriers can be triggered by ultrasound, which
accelerates percolation of the drug molecules through the pores via low-frequency
oscillations and cavitation effects (Ahmed et al. 2021; Wan et al. 2021).
The application of high-intensity focused ultrasound (HIFU), as distinct from
low-intensity ultrasound, induce s hyperthermic effects and when used in combination with thermosensitive drug carriers, enables spatiotemporally controlled drug
release. One example is the combination of HIFU with the liposomal doxorubicin
formulation ThermoDox (Celsion Corp.), currently investigated in clinical trials for
the treatment of hepatic tumours, sarcoma, and bone metastasis. Other types of
thermoresponsive nanocarriers, such as micelles, solid–lipid nanoparticles, or coreshell nanoparticles, utilizing thermosensitive lipids and polymers, are being investigated in combination with HIFU for on-demand drug release.
In an innovative approach, carboxyl-calcium coordination bonds were incorporated in the sodium alginate coating of MSNs, which blocked the pores of MSNs and
prevented the cargo from being released before stimulation. The coordination bonds
would break upon exposure to low-intensity ultrasound (at 20 kHz) or HIFU
(at 1.1 MHz), leading to rapid payload release. When ultrasound exposure is paused,
416 N. Nomikou et al.
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the coordination bonds can be reformed, suspending the payload release process
(Li et al. 2019). This controllable drug release system demonstrates the potential of
ultrasound to serve as an on–off switch in a remote and site-specific manner.
15.4 Conclusions
The array of stimulus-responsive nanosystems designed and developed, thus far,
holds significant potential to improve the efficacy and targeted effects of therapeutic
modalities for different disease types, by providing spatiotemporally controlled drug
release. Importantly, using combinations of the smart design and structural functionality approaches described in this chapter, nanosystems that are responsive to
more than one stimulus can be constructed for multimodal or multidrug delivery
(An et al. 2016; Hegazy et al. 2017; You et al. 2018). Using these dual- or multiresponsive systems, different agents can be released from nanocarriers at different
times and/or the timing of payload release from a nanoparticle does not need to
coincide with payload activation. It is impo rtant to note that this chapter focuses on
the responsiveness of the actual nanocarrier systems and does not cover the concepts
of photodynamic and sonodynamic therapies, which involve the activation of
non-toxic agents, called sensitizers, using light and ultrasound, respectively (McHale
et al. 2016; Kwiatkowski et al. 2018). The stimulus-responsive nanocarriers
described here still carry chemotherapeutic or other toxic-to-healthy tissue agents,
which off-target tissues/organs, such as liver, kidneys, and spleen, are heavily
exposed to, with subsequent side effects. Importantly, drug delivery using
nanoparticles in the treatment of solid tumours still heavily depends on the
hyperpermeable vasculature and suppressed lymphatic clearance characteristic of
tumour tissues, known as the EPR effect. This effect can guarantee the accumulation
of only a small proportion of the nanoparticles within the tumour mass, while there is
significant accumulation in peripheral organs and tissues. The endogenous and
exogenous stimuli can provoke drug release from nanoparticles that have already
accumulated in the tumour mass through the EPR effect. Hence, the dose, frequency,
and duration of systemic administration are still restricted, despite the spatiotemporal
control that stimulus-responsive systems offer. One additional aspect to consider in
terms of the clinical translation of each system is the fact that the nanocarriers and
their drug release mode alter drug efficiency and consequently, doses of drugs need
to be recalibrated.
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