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302 M. E. Lane and A. Rahma
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and about 50–150 nm in length) in an in vivo mini pig study. Preparations were
applied four times daily, 5 days a week for a total of 22 days. At the end of the study
period, skin samples were analysed via TEM and Scannin g Electron MicroscopeEnergy Dispersive X-Ray spectroscopy, and blood samples were measured using
Inductively Coupled Plasma Mass Spectrometry. All three types of NPs were
concentrated in the SC layer. There was no evidence of follicular penetration and
e d
in th
ermis, only a few isolated NPs were observed.
Gulson et al. (2010) applied two types of ZnO NP to human volunteers: a
preparation containing 19 nm NP or a vehicle containing 100 nm NP. Stable isotope
tracing with
68
Zn was used to distinguish dermally absorbed Zn from endogenous
Zn. Although Zn was detected in the blood after 5 days, it was not possible to
determine whether the levels represented Zn absorbed as intact particles or soluble
Zn or both. Van der Merwe et al. (2009) investigated the in vitro penetration of
magnesium oxide (7 nm thickness, 100 to 200 nm in length) and TiO
particles
2
(<1 nm crystallites which aggregate into micron size particles of 5 μm) in
dermatomed human skin. Application of the particles as a dry powder, water
suspension, and suspensions with 0.2% w/v sodium lauryl sulphate (SLS) for
8 hours did not result in any absorption of the particles through the skin. Iron
oxide (γ-Fe
) particles (5.9 nm) coated with tetramethyl ammonium hydroxide
2O3
(TMAOH) were evaluated in human skin in vitro by Baroli et al. (2007).
Nanoparticles were observed to penetrate into the stratum corneum and hair follicles
but did not permeate through the skin.
Mohammed et al. (2019) have studied the safety of repeated application of
agglomerated zinc oxide (ZnO) NPs to human volunteers over 5 days. Skin penetration of intact ZnO NPs and
zinc ions was assessed using multiphoton tomography
with fluorescence lifetime imaging microscopy. ZnO NPs accumulated on the skin
surface and within the skin furrows but did not enter or cause cellular toxicity in the
viable epidermis. Zinc ion concentrations in the viable epidermis of excised human
skin were slightly elevated. The authors concluded that repeated application of ZnO
NPs to the skin, as used in global sunscreen products, appeared to be safe with no
evidence of toxicity in the viable epidermis. More recently, similar findings were
confirmed by Khabir and colleagues (2021). These authors quantified the relative
concentrations of endogenous and exogenous Zn using a rare stable zinc-67 isotope
after application of ZnO NPs to excised human skin. ZnO NPs were retained on the
skin surface or confined to the outer layers of the skin; dissolved zinc species
permeated across the SC into the VE as ionic Zn and not as ZnO NPs.
Metal Nanoparticles
The permeation of iron nanoparticles (4.9–23.3 nm) was evaluated in full-thickness
human skin in vitro by Baroli et al. (2007) using a vertical diffusion cell experimental design. Iron deposits were observed below the viable epidermis and within and
proximal to the hair follicles; however, the NP did not permeate through the skin.
Gold core particles with silica shell s (94 ± 6 and 161 ± 13 nm) and silica particles
coated with a gold shell (298 ± 11 nm) were applied to human skin samples by Graf
et al. (2009). Scanning transmission X-ray microscopy confirmed that particles with
12 Non-deformable Nanoparticles and Transdermal Penetration 303
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dimensions 161 ± 13 nm were observed in the superficial layers of the stratum
corneum and hair follicles but no deeper penetration was observed. Filon et al.
(2007) and Larese et al. (2009
nanoparticles (9.8–48.8 nm)
presence of nanoparticles solely in the lower layers of the stratum corneum using
Transmission Electron Microscopy. Samberg and co-workers (2010) evaluated
in vivo porcine exposure to silver nanoparticles (20–50 nm) over 14 days at varying
dosages. After 14 days of topical dosing, TEM confirmed that NP could only be
found in the superficial l
penetration of silver nanoparticles in pig and human skin. A mass balance study in
human skin found that most nanoparticles were washed from the skin or remained in
the stratum corneum.
Nanoparticles Fabricated with Polymeric Materials and Starch
Polymerized lactic acid (PLA) and polymerized glycolic acid (PGA) and the related
co-polymer poly-lactide-co-glycolide (PLGA) are used to formulate implants and
other injectable medicinal products. Various studies have investigated whether
nanoparticles fabricated with these polymers might enhance (trans)dermal delivery
of actives. Luengo and co-workers (
nanoparticles (mean size 328.2 nm). Enhanced transport and higher accumulation of
fluefenamic acid compared with unencapsulated drug was observed in excised
human skin in Franz cell studies after ~24 h. Although particles were found
homogeneously distributed on the skin surface and within the skin folds, no
nanoparticles were detected within or between the corneocytes. The penetration
and storage behaviour of 5-fluoresceinamine-labelled PLGA nanoparticles (diameter
320 nm) in porcine skin in vitro and human skin in vivo was evaluated by Lademann
et al. (2006, 2007). NP did penetrate deeply into the hair follicles of human skin but
only penetrated the upper two layers of the SC. After 10 days, NP could still be
detected in the hair follicles, but the residence time in the SC was only 24 h.
However, in these experiments, the formulations were rubbed into the skin with a
massage device rather than simply being applied to the skin sites and this is likely to
contribute significantly to the apparent uptake of the NP by the skin.
) investigated the percutaneous absorption of silver
in human skin in vitro. The authors reported the
ayers o
f the SC. Kraeling et al. (
2006) encapsulated flufenamic acid in PLGA
2018)
examined
the
in
vitro
Tsujimoto et al. (2007) investigated PLGA nanoparticles (205 nm) for delivery of
hinokitiol to hair follicles. Using human scalp biopsy samples and confocal laser
microscopy (CLM), the PLGA nanoparticles appeared to deliver more of the
hinokitiol to a greater depth in the scalp. No permeation data were reported in the
study. Rancan et al. (2009) investigated the penetration of fluorescent dye-loaded
PLA particles (228 and 365 nm) in human skin explants. Particles did not permeate
the follicular epithelium to the viable tissue but did accumulate in hair follicles.
Vettor et al. (2010) investigated the skin distribution of octyl-methoxycinnamate
(OMC) from PLA nanoparticles compared with an OMC emulgel formulation using
Franz cell diffusion studies. The amount of OMC released from NP to viable skin
was threefold lower than from the emulgel but the fate of the NP was not evaluated.
The penetration profile of 40, 750, and 1500 nm fluorescent polys tyrene NP in
human skin samples was investigated by Vogt and co-workers (2006). NPs were
304 M. E. Lane and A. Rahma
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Fig. 12.4 Schematic of interaction of NPs of different sizes on the skin
applied for 15–16 h at 37 °C. The larger particles aggregated in the hair follicle
openings; only 40 nm particles entered the hair follicle openings and penetrated the
follicular epit helium. Skin disposition and permeation of polystyrene and poly
(methyl methacrylate) NP was examined in vitro using dermatomed porcine skin
by Wu et al. (2009b
). The fluorescent tag, fl
uorescein methacrylate (FMA), was used
to label the polymers, and a second fluorescent compound, Nile Red, was loaded into
the particles. The mean diameter of the polystyrene NP was <50 nm while the poly
(methyl methacrylate) NPs were approximately twice as large. In vitro skin permeation experiments were conducted over 6 h. While NPs did accumulate in skin
furrows and on and around hair follicles, they did not penetrate beyond the outer skin
. I
layers
n a later study, the infl
on topical delivery of Nile Red to porcine skin was examined (Wu et al.
Three poly-(ε-caprolactone)
uence
NP
particle size and polymer hydrophobicity
of
2009c).
(CAPA) formulations (90, 260, and 630 nm) loaded
with NR were used to study the impact of particle size on delivery of the model
active. The larger NPs were more efficient at delivering NR into the skin, presumably because of the larger area of exposure to the skin (Fig.
12.4).
In a late r study, Wu et al. (2010) investigated the interaction of three types of
charged nanoparticles after application to porcine skin in vitro. NPs were formulated
with a cationic amino-functionalized polystyrene (PS-[+]), an anionic carboxylfunctionalized polystyrene (PS-[-]), and an anionic PLA polymer (PLA-[-]).
Particles were loaded with fluorophore N-(2,6-diisopropylphenyl)perylene-3,4dicarboximine (PMI). The cationic nanoparticles showed clear affinity for the
negatively charged skin surface, in contrast to the anionic nanoparticles. The cationic
NP also delivered a significantly greater amount of the PMI into the SC. The affinity
of NP for hair follicles was also confirmed.
Zou and colleagues (2017) studied the interaction of three different -sized polystyrene NPs marked with red fluorescence with human skin, with Calcium Green 5 N
used as a counterstain. Dimethyl sulfoxide (DMSO) and ethanol were used as
alternative vehicles for NPs. Tape stripping was utilized as a barrier-damaged skin
model. Skin biopsies dosed with NPs were incubated at 4 °C or 37 °C for 24 h and
imaged using confocal laser scanning microscopy. NPs were localized in the stratum
corneum (SC) and hair follicles without penetrating the epidermis/dermis. Barrier
alteration with tape stripping and change in incubation temperature did not induce
deeper penetration. Using horizontal scanning by 2-photon microscopy (2 PM) of
full-thickness human skin samples, Dogt and co-workers (2018) demon strated that
12 Non-deformable Nanoparticles and Transdermal Penetration 305
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fluorescently tagged 20 and 200 nm polystyrene nanoparticles preferentially accumulated in the stratum corneum (SC) and in the upper part of vellus hair foll icles
(HFs). Deeper penetration into the viable epidermis and HF infundibulum of 20 and
200 nm nanoparticles at sites of high focal parti cle aggregation was reported by the
authors. However, it is important to note that this study used excised scalp skin and it
is not clear if the method of preparation of the skin sampl
tissue.
Santander-Ortega et al. (2010) formulated NP composed of propyl-starch derivatives of varying degrees of substitution (PS-1 and PS-1.45) and encapsulated three
drugs (flufenamic acid, testosterone, caffeine) in the NP. Although drug permeation
was observed for all NPs, this was not improved for testosterone and caffeine
compared to permeation of drug alone and the authors did not investigate the fate
of the NP in skin.
Quantum Dots and Fullerenes
Quantum dot NP (semiconductor nanocrystals) are inherently fluorescent and are
available in sizes <10 nm. The permeation of two types of quantum dot NPs in
porcine skin in vitro (spherical NP with a diameter of 4.6 nm and ellipsoid NP with
major axis of 12 n m and minor axis of 6 nm) was investigated by Ryman-Rasmus sen
et al. (
2006). The NPs were also prepared with neutral, cationic, and anionic
coatings. Prior to application to porcine skin in diffusion cells, the NPs were
suspended in borate buffer of pH 9 or pH 8.3. Neutral and anionic NPs were detected
in the epidermis and cationic NPs were observed in the dermis using confocal
microscopy imaging. The buffer systems may have contributed to skin damage
during the experiment and are not representative of typical vehicles that are applied
to human skin. The same group (Zhang et al. 2008) evaluated in vitro porcine skin
permeation of nail-shaped quantum dot NP (QD621) composed of a cadmium/
selenide core, a cadmium sulphide shell, coated with PEG and with a hydrodynamic
diameter of 39–40 nm. NPs were determined in the SC and in the superficial areas of
the hair follicles after 24 h but not in the dermis. Jeong et al. (2010) applied QD
under occlusion to the arm of human volunteers for 4 h. NPs were found in the SC
layers after tape stripping but NP penetration of the SC was not demonstrated.
es may have damaged the
The interaction of cadmium telluride (CdTe) QD (~3.5 nm) with human skin
in vitro was investigated by Gratieri et al. (2010). The effects of massaging and
artificial damage of the skin by tape stripping were also explored. Non-invasive
multiphoton spectroscopy, CLM, and sectioning of the SC followed by CLM were
used to evaluate QD depth profiles. The formulation and skin were left in contact for
15 h before analysis. Although massaging the skin clearly altered the distribution of
QD in the skin samp les, there was no evidence of penetration into the skin. Tapestripped skin did indicate enhanced QD uptake (7 μm depth) into the skin.
Nastiti and colleagues (2019) examined the influence of biological factors such as
age and anatomical site on the penetration and distribution of 2.1 nm hydrophilic
CdTe/CdS quantum dots: QDs in adult pig skin (APS), weanling pig skin (WPS),
and new born pig skin (NBPS) at two different anatomical sites (ear and abdomen).
After 6- or 24-h incubation on Franz diffusion cells, tape stripping of skin was
306 M. E. Lane and A. Rahma
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conducted. QDs were mainly localized in h air follicles after 6 and 24 h of exposure
with no cadmium detected in the Franz cell receptor compartment regardless of pig
age or anatomical site. The amount of QDs deposited in the follicles was similar at
6 h but higher on APS and WPS ears compared to NBPS ears at 24 h. This is
associated with the high follicle density and small follicle diameter of the NBPS
compared to the smaller density of much larger follicles on the APS. NBPS showed
onsis
tent QD distribution for ear and abdomen up to 24 h. The authors concluded
c
that
there
min
imal penetration of QDs through pig skin.
is
Fullerenes are composed of carbon and may have spherical, ellipsoid, or tube-like
structures. Rouse et al. (2007) synthesized a fullerene-substituted peptide (CarbonBAA-Lys-[FITC]-NLS) and evaluated its penetration through flexed and unflexed
porcine skin in vitro. After 60 or 90 min flexing the skin was mounted in diffusion
cells and percutaneous absorption was assessed over 8 and 24 h. Confocal microscopy confirmed dermal penetration of the flexed skin by 8 h but no dermal penetration of unflexed skin was observed until 24 h. Kato and co-workers (
2009) applied
three different doses of fullerene-60 in a squalene vehicle to human skin in diffusion
cells for 24 h. Following tissue extraction and analysis, fullerene-60 was detected in
the epidermis but not in the dermis. Xia et al. (
2010) applied pristine fullerenes in
mineral oil, toluene, cyclohexane, or chloroform to the dorsal area of pigs for 24 h.
Fullerene was not detected in the skin when dosed in mineral oil but when dosed in
toluene, cyclohexane, or chloroform, fullerene penetrated deeply into the skin. The
rationale for selection of some of the solvents used in the study must be questioned
because of their known ability to disrupt the skin lipids.
12.6 The Penetration of Nanoparticles in Human Skin:
A Theoretical Perspective
Assuming that NPs behave like large molecules, it is possible to estimate their rate of
penetration using simp le diffusion theory (Watkinson et al. 2013). To demonstrate
this approach, a hypothetical spherical molecule of molecular weight 500 and log
K of 2 should be considered. Assuming a density of 1 g/cm
be 500 cm
3
/mole and correcting for Avogadro’s number gives the volume of an
individual molecule 8.3 × 10
0.58 nm.
The Potts and Guy relationship, discussed in Sect. 3.2, relates permeation to an
exponential function of molecular weight or molecular volume. This allows the
prediction of permeability coefficients (k
into aqueous solutions (Potts and Guy 1992), using the octanol water partition
coefficient (K ) and the molecular weight (M). Even though this relationship was
developed from a limited data set in terms of molecular weight (18–765), it should be
possible to extrapolate to consider NP penetration. When some NPs of different
diameters are considered and using the same approach as taken for the hypothetical
-22 cm3
3
, the molar volume will
. From this the estimated molecular radius is
) across the skin for chemicals dissolved
p
12 Non-deformable Nanoparticles and Transdermal Penetration 307
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Table 12.1 Predicted permeability coefficient values (k
) for NPs of varying dimensions calculated
p
from the Potts–Guy equation relationship
Particle
diameter (nm)
1 5.2 × 10
2 4.2 × 10
5 6.6 × 10
Particle
volume (cm
-22
-21
-20
Volume of 1 mole
3
)
particles (cm
3
)
Molar mass
(g/mole)
log
(k
/cm2 s
p
-1
)
315 315 -6.80 1.57E-07
2523 2523 -20.3 5.38E-21
39,419 39,419 -245 4.61E-246
(kp/cm2 s
-1
Assuming Log K of 2
Table 12.2 Predicted J
Particle
diameter (nm)
Molar mass
(g/mole)
1 315 - × 10
2 2523 -40 8 × 10
values for NPs of various dimensions calculated using Eq. 12.2
max
log
(J
max
91
/mol cm
-2 h-1
) J
/mol cm
max
-9
-41
-2 h-1
J
max
341
2 × 10
/ng cm
-28
-2 h-1
5 39,419 -560 0 0
Assuming Log K of 2
molecule the data in Table 12.1 can be generated. A further assumption is that the
particles partition favourably into the skin with a log K value of 2 which is optimum
for a molecule to partition across the heterogeneous structure of the skin and into the
systemic circulation.
An alternative approach is to use the algorithm of Magnusson et al. (2004). In this
publication, the authors relate the maximum flux (J
/mol cm
max
-2 h-1
) across the
skin to molecular weight. Considering the NPs of the same dimensions as for the
previous calculation, this then allows the values reported in Table
12.2 to be
calculated for the maximum flux across the skin.
It is evident that as the size of the non-deformable NP increases, the amount that
can penetrate the skin becomes increasingly small. Importantly, the two approaches
to estimate the rates of permeation of nanoparticles are consistent but it is important
to note that they are derived on the same types of data sets. It follows then that if
penetration through skin of intact NPs occurs, then it is not a passive diffusion
process.
)
12.7 Summary
In this chapter, the interaction of non-deformable NP with the skin has been
reviewed. Most of the studies considered indicate that such NPs only permeate the
superficial layers of the skin, that is, the SC. Very limited evidence is presented for
epidermal penetration and dermal absorption. Where epidermal permeation was
observed, it is generally associated with mechanical stress or relatively harsh
308 M. E. Lane and A. Rahma
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vehicles or where the skin is artificially damaged. Follicular penetration is suggested
as a possible route of non-deformable NP permeation. However, the hair shaft itself
is known to move under normal in vivo conditions, and the extent to which this may
influence any possible follicular permeation needs to be carefully evaluated. A
theoretical framework to understand the factors that determine and limit solid nondeformable NP penetration in the skin is consistent wit
h the experimental findings
reported in the literature.
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