Journal of Colloid and Interface Science 567 (2020) 224–234

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Journal of Colloid and Interface Science

journal homepage: www.elsevier.com/locate/jcis

Spreading of biologically relevant liquids over the laser textured surfaces

A.M. Emelyanenko, L.B. Boinovich ⇑, K.A. Emelyanenko
A.N. Frumkin Institute of Physical Chemistry and Electrochemistry, Russian Academy of Sciences, Leninsky prospect 31 bldg. 4, 119071 Moscow, Russia

h i g h l i g h t s g r a p h i c a l a b s t r a c t

Spreading on the laser textured

surface shows the formation of three
spreading fronts.

The anisotropy of spreading for all
types of liquid fronts was found.

Biologically relevant liquid imbibition
into the nanotexture follows
universal power law.

a r t i c l e i n f o a b s t r a c t

Article history: Hypothesis: The distribution of biological objects upon the spreading of biologically relevant dispersions
Received 20 November 2019 over laser textured surfaces is affected by the dispersion composition and substrate chemistry and
Revised 2 February 2020 roughness.
Accepted 3 February 2020
Experiments: To examine the role of the substrate texture in biologically relevant liquid spreading, the
Available online 6 February 2020
dynamic behavior of droplets of water and dispersions of bacterial cells and viruses and dynamic behav-
ior of droplet/air surface tension were addressed. A new procedure to simultaneously distinguish three
Keywords:
different spreading fronts was developed.
Textured surface
Contact angle
Findings: The study of spreading of water and the biologically relevant liquids over the laser textured
Wetting substrate indicate the development of three spreading fronts associated with the movement of bulk dro-
Spreading plet base, the flow along the microchannels, and the nanotexture impregnation. The anisotropy of spread-
Roughness ing for all types of liquid fronts was found. Despite the expected difference in the rheological behavior of
Dynamic wetting water and the biologically relevant liquids, the spreading of all tested liquids was successfully described
Biologically relevant liquid by power-law fits. The droplet base spreading for all tested liquids followed the Tanner law. The advanc-
E. coli ing of water and dispersions in the microchannels along both fast and slow axes was described by
Bacteriophage
Washburn type behavior. The impregnation of the nanotexture by water and biologically relevant liquids
Image processing
demonstrated universality in power fit description with an exponent n = 0.23.
Ó 2020 Elsevier Inc. All rights reserved.

1. Introduction and spreading of biologically relevant liquids is an important area

Biologically relevant liquids are ubiquitous and are present in
various areas of human activity. Typical examples of such liquids
are dispersions of cells, proteins or viruses. Control of wettability
⇑ Corresponding author.
E-mail address: boinovich@mail.ru (L.B. Boinovich).
of laboratory research not only for fundamental scientific reasons
but also because of their significance for a broad range of indus-
trial, including medical and food applications. One of the most
intensively developed areas in the manufacturing of functional
materials is the design of coatings with a bactericidal effect
[1–5]. For such coatings, fast spreading of dispersion of bacterial
cells or viruses along the surface with the uniform distribution of
biological organisms is an important step for obtaining the

https://doi.org/10.1016/j.jcis.2020.02.006
0021-9797/Ó 2020 Elsevier Inc. All rights reserved.
 A.M. Emelyanenko et al. / Journal of Colloid and Interface Science 567 (2020) 224–234
appreciable bactericidal effect [4,6]. The surfaces with multimodal
roughness based on nano- and microelements of the texture, are
considered as the most promising for control of spreading peculiar-
ities and bactericidal functionality. One may find numerous exper-
imental and theoretical studies devoted to the investigation of
spreading of Newtonian liquids along the smooth [7–17] and
roughened substrates [18–26], as well as inside the microchannels
of different shapes [27–30]. It was shown that spreading of the
bulk part of the droplet is defined by the interplay of inertial, grav-
itation, and capillary effects, which act as driving forces balanced
by viscous effects and solid/liquid friction effects resisting the
extension of the bulk liquid front.
For completely wetting droplet of a Newtonian liquid on a
smooth homogeneous substrate, beyond the quick spreading ruled
by inertia, two spreading regimes should be considered. When a
radius of the droplet is less than the capillary length and capillary
forces on the droplet surface are dominating, the time evolution of
droplet base radius, Rb, obeys the law Rb(t) ~ {(r/g)V3t}1/10, where
V, r and g are the droplet volume, liquid surface tension, and the
liquid viscosity, respectively. As the droplet radius grows beyond
the capillary length, the domination of the gravity force causes
the droplet flattening. At this stage, the droplet base radius grows
as Rb(t) ~ {(qg/g)V3t}1/8, where q is the density of the liquid and g is
the gravitational acceleration. The spreading of the bulk liquid
front atop of substrate is preceded by a precursor film of molecular
dimensions [7,31–35], whose advancement follows the diffusion
dynamics according to Rb(t) ~ t1/2.
The situation becomes far more complicated when the
spreading over roughened surfaces is considered. Impregnation
of micro- and nano-sized topographic features, which form
multiple capillary channels with different excess pressures inside
the liquid bridges, modifies the spreading rate of liquids. For such
surfaces, droplet spreading is determined by the complex interplay
of gravitational contributions, capillary contributions both inside
the droplet and within capillary channels, surface forces, and vis-
cous/friction dissipation. Besides, the particular combination of
the substrate surface energy and the surface relief may cause the
replacement of a homogeneous wetting regime by the heteroge-
neous one, which in turn will contribute to the rate of liquid fronts
propagation. The most studied situation corresponds to the
spreading of liquid on a surface with random or periodic grooves
or channels [27–30,36,37]. Various experimental and theoretical
studies have shown that for liquids, completely wetting the groove
walls, liquid front spreading along the groove advances as t1/2. Such
dependence was observed for open grooves with different geome-
tries [27,30,36–41] and for liquid-liquid displacement [28]. Thus,
the spreading scenario for the Newtonian liquid droplet atop of
the composite textured substrates is rather complex.
In our recent study, we have shown for laser-textured sub-
strates the power-law isotropic spreading of a bulk part of a
hexane droplet, Washburn type anisotropic propagation of liquid
over microgrooves, and anisotropic impregnation of the nanotex-
ture. The situation becomes much more intricate when the
spreading of a non-Newtonian liquid, in particular, the biological
fluid containing cells or viruses, is considered. So far, studies
devoted to the spreading of biologically relevant liquids are
scarce. In this paper, we present the results of comparative study
of water and biologically relevant liquids spreading over the
laser textured substrate. Here, the diluted suspensions of bacte-
rial cells of Escherichia coli (E. coli) strain and bacteriophages in
aqueous dispersion medium were used as biologically relevant
liquids. The observed peculiarities of spreading make it possible
to better understand the rheological behavior of bacterial cells
and viruses upon suspension spreading and open a way to
purposefully manage the interaction of cells or viruses with
the substrate.
225
2. Materials and methods
2.1. Materials
The droplet spreading experiments were conducted at room
temperature on substrates obtained by laser texturing of
aluminum-magnesium alloy AMG2 (Neva Metal LLC, Russia). The
peculiarities of spreading of the biologically relevant liquids were
studied using the deionized water (electrical conductivity
1.2  106 X1 cm1, pH = 6.3), and the dispersions of the bacteria
at a titer of 1  107 CFU/mL and the bacteriophage at titers of
1  107, 1  108, and 1  109 PFU/mL in a physiological solution
(0.9% NaCl aqueous solution, pH of 7.4). Hereinafter, CFU and PFU
stand for colony-forming units and phage-forming units,
respectively.
In this study, we used a nonpathogenic strain E. coli K12 C600
(‘‘GCPM-Obolensk”, B-7158, Obolensk, Russia) and the original vir-
ulent polyvalent bacteriophage E. coli BPhEc1 (EcD7) (‘‘DSMZ”, DSM
28572, Braunschweig, Germany). The typical size of mature E. coli
bacteria is 0.9–1.0 lm in diameter and 2–5 lm in length [42]; bac-
teriophage EcD7 has a capsid diameter of 21–22 nm [43].
The protocols of strains growth and handling were described in
detail in [4]. Briefly, the desired titer of E. coli was obtained by
sequential 10-fold dilutions with physiological solution of fresh
overnight cultures incubated at 37 °C and prepared on Luria–Ber-
tani broth with opacity standard corresponding to 1  109 CFU/
mL. In order to create reproducible conditions, the cells were sep-
arated from the used culture medium after cultivation and were
resuspended in fresh physiological solution to obtain a defined cell
concentration. Bacterial titer was controlled at all stages of the
study by parallel inoculation of 0.1 mL samples of the dispersion
used in the experiment on Mueller–Hinton agar. A highly active
sterile phage lysate purified from toxins was produced using the
pilot technology [44] with E. coli K12 C600 as a host strain for
the bacteriophage EcD7. Bacteriophage titer in the dispersion was
controlled by the Gratia method [45] on an 18 h (fresh overnight)
E. coli K12 C600 culture.
2.2. Substrate preparation
Flat sheets of AMG2 alloy with dimensions 40  40  1 mm3
were degreased in a 1 M KOH solution, ultrasonically washed in
deionized water and dried with ash-free filter paper.
Laser treatment was performed in ambient conditions with
humidity of 40–50% and temperature of 20–25 °C using an infrared
laser system (Argent-M, LTC LLC, Russia) with an IR ytterbium fiber
laser (wavelength 1.064 lm) and a 2-axis laser beam deflection
unit (MS10, Raylase GmbH, Germany). In the course of laser pro-
cessing, the samples were raster-scanned by a focused beam
(40 lm wide), at a linear speed of 50 mm/s with parallel line pitch
of 0.02 mm, a pulse duration of 50 ns, the repetition rate of 20 kHz
and peak power of 0.95 mJ in TEM00 mode as described in [46].
2.3. Substrate characterization
The freshly fabricated samples demonstrated fast aqueous and
hydrocarbon liquids spreading and complete wicking. To estimate
the Young contact angles for the laser-textured samples (that is,
the intrinsic wettability of Al2O3, aluminum oxide constituent of
the micro- and nano- surface textures), we have used the polished
sapphire plates from Knight Optical (Kent, UK) as the model Al2O3
surfaces. To quantitatively characterize the obtained hierarchical
texture, the wettability of samples after chemisorption of fluorosi-
lanes (as described in [46]) was measured. In order to characterize
the contact and roll-off angles for such hydrophobized substrates,
226 A.M. Emelyanenko et al. / Journal of Colloid and Interface Science 567 (2020) 224–234
the 15 mL droplets of water or biologically relevant liquids were
used. The contact and roll-off angles were measured at least 5
times in different places of the substrate for each liquid. The con-
tact angles and a surface tension of a sessile droplet of a testing liq-
uid were measured using a custom-designed experimental setup
basing on the digital processing of droplet images and Laplace fit
optimization for determining the droplet shape parameters. The
details of such measurement were presented in [46,47]. The roll-
off angles for water droplets were defined upon gradual substrate
tilting and finding the inclination angle at which the droplet
started to move along the surface.
For the sessile droplets of aqueous liquids deposited onto the
superhydrophobic surface the continuous monitoring of the evolu-
tion of droplet surface tension becomes possible. This, in turn,
allowed analyzing the surface activity or, by other words, the
propensity of bacterial or bacteriophage culture to be accumulated
at the liquid-air interface, which is initiated by a tendency to
decrease the energy of the considered system. To monitor the dro-
plet surface tension, the dispersion droplet was deposited onto the
superhydrophobic substrates and kept in saturated water vapor
conditions using the double-wall cell described in [48].
The measurements of the density and the dynamic viscosity of
water and biologically relevant dispersions were performed using
viscometer SVM 3001 (Anton-Paar, Austria). The measurements
were repeated 10 times, each time for a new portion of liquid.
The morphology of the sample surfaces was studied using a
scanning electron microscope (SEM) Supra 40 VP (Carl Zeiss AG,
Germany). Micrographs were taken at 2–5 kV acceleration voltage
using a secondary electron detector.
2.4. Spreading studies
The studies of the spreading kinetics were performed in the
conditions of a nearly saturated water vapor atmosphere. Photo
and the scheme of the experimental setup for recording optical
images of the top view of spreading droplets are presented in
Fig. 1. A substrate with spreading droplet was located inside the
polystyrene experimental cell with transparent glass cover. The
high precision dosing system LSP01-1A (Longer Precision Pump
Co., Ltd, China) with a long needle was used to deliver a liquid dro-
plet of definite volume onto the substrate. To reach the saturated
water vapor conditions, the wet sheets of filter paper were
attached to the polystyrene cell walls. The experimental cell was
Fig. 1. Experimental setup for studying spreading of liquid over textured substrates: general view (left panel) and the scheme (right panel). 1 – sample with spreading
droplet; 2 – polystyrene box; 3 – glass cover; 4 – syringe dosing system; 5 – leveling table; 6 – microscope; 7 – video camera; 8 – computer.
placed onto a precisely leveling optical table. Optical images of
the spreading droplet formed in an optical microscope Stemi
SV11 (Zeiss, Germany) were captured by high-speed digital camera
(FL3-U3-13S2M-CS, Point Grey Research Inc., Canada) and stored in
the computer. The liquid droplets volume in all reported experi-
ments was 6 mL.
To define the coordinates of points associated with the position
of different spreading fronts, we used the method of digital video
image processing. We would like to stress the new experimental
possibility, developed in our study, and related to the analysis of
liquid spreading along the rough substrates with multimodal (hier-
archical) roughness. Namely, the procedure to simultaneously dis-
tinguish three different spreading fronts (Fig. 2), associated with
the propagation of liquid through the nanofeatures and along the
microchannels, and with the movement of bulk droplet base, were
developed. The highest expanding rate was detected for the first
front mentioned above, which arises due to the capillary impreg-
nation of a substrate nano-texture by a precursor film. The forma-
tion of the microchannels/microgrooves upon laser texturing
causes the directional propagation of liquid along these channels
and the appearance of the second liquid front with the spreading
velocity lower than that for the first one. Spreading of a droplet
base over the rough substrate impregnated with the same liquid
is associated with the third front. To enhance the precision of the
detection of different front positions, we have used two software
procedures developed in our previous study [39] for sequential
digital image processing of different fronts (Fig. 2a). According to
[39], for reliable positioning of the outer front associated with
the capillary impregnation of a substrate nanotexture with a pre-
cursor film, the differential image should be used. Such image is
obtained as a result of the difference in the intensity of scattered
light for each pixel in the field of the image for the substrate with-
out droplet and the substrate with the spreading droplet (Fig. 2b).
A higher contrast for detection of this front is based on the depres-
sion of light scattering from the nanorough surface upon its filling
with a liquid resulting in luminous precursor film atop of black
background (Fig. 2b).
The detection of the positions of liquid fronts, corresponding to
the propagation of liquid along the microchannels and the
advancement of the bulk droplet base was performed using the
second type of procedure. It was based on the analysis of differen-
tial images (Fig. 2c) obtained by pixel-by-pixel subtraction of the
intensity of scattered light for the substrate with the spreading
 A.M. Emelyanenko et al. / Journal of Colloid and Interface Science 567 (2020) 224–234 227

Fig. 2. Illustration of developed procedures for digital processing of video images of spreading droplets. (a) Optical image of the spreading droplet on the textured substrate;
(b) after applying the difference filter enhancing the position of outer front of the wet spot (solid line); (c) after applying the subtraction filter simplifying the detection of bulk
droplet base (dotted line) and of the front, associated with the propagation of liquid along the microchannels (dashed line).

droplet and that for the substrate without droplet. This procedure
is based on the local increase in intensity of reflected light either
due to the filling of microchannels with a liquid or due to droplet
flattening upon its spreading. The application of digital image pro-
cessing with abovementioned software procedures to the analysis
of the evolution of liquid spot on the differential images for each
studied droplet allows simultaneous and more accurate detection
of different spreading fronts. Using the abovementioned approach,
we performed spreading experiment thrice for each test liquid to
obtain the statistically reliable results.
3. Results and discussion
view SEM images at different magnifications. The combination of
regular surface ripples and trenches (Fig. 3a), with globule-like
aggregates composed of nanoparticles and capsule-shaped densely
packed micro- and nanopores (Fig. 3d and Fig. S1 in the Supporting
Information) clearly indicate the formation of multimodal surface
texture with micro and nanochannels. The analysis of the texture
allows concluding the formation of a set of long, nearly parallel
channels interconnected by the randomly distributed short trans-
verse trenches. To visualize the channels and trenches we applied
to the image Fig. 3a a binarization procedure using variable grey-
scale thresholding. This procedure allowed selecting deeper sec-
tions of textured surfaces as marked by blue color in Fig. 3b.

3.1. Fabricated surface morphology
At chosen regime of laser treatment, the interaction of the laser
beam with the substrate leads to formation of multimodal rough-
ness of used substrates. The obtained morphology is characterized
in detail in Fig. 3 by the top (a,b), tilted (c), and cross-section (d)
3.2. Wettability studies and the analysis of the surface activity of the
biological objects
It is important to stress that due to multimodal roughness, our
substrates were completely wetted by water. To elucidate the role
of the chemical structure of oxidized aluminum surface used as a

Fig. 3. SEM images of the laser-textured surface of AMG2 samples at various magnifications. (a, b) top view; (c) tilted view; (d) cross-section view. To visualize the channels, a
binarization procedure with variable greyscale thresholding was applied to the image (a) with deeper sections of surface texture marked by blue color in (b); for reference on
color in this figure the reader is addressed to the online version of the article.
228 A.M. Emelyanenko et al. / Journal of Colloid and Interface Science 567 (2020) 224–234

basis for substrate preparation, we have measured water and

biologically relevant dispersion contact angles for polished
sapphire plates used as the model Al2O3 surfaces. Due to the
superhydrophilic state of the substrate after laser texturing, the
impact of the texture itself is difficult to analyze quantitatively
for the substrate just after texturing. However, after modification
of the textured surface by fluorooxysilane and attaining the super-
hydrophobic state of the surface, the difference between water and
biologically relevant liquids in the wettability characteristics
related to the peculiarities of the texture can be easily detected.
Besides, tracing the surface tension of sessile droplet of biologically
relevant liquids on the superhydrophobic surface in time allows
getting the unique possibility to analyze the surface activity of bac-
terial cells or bacteriophages. Such surface activity is a determining
factor for the evolution of droplet surface tension in time and its
influence on the spreading behavior.
As follows from the data in Table 1, the Al2O3 surface is hydro-
philic. The laser roughening of such substrate, in accordance with
the Wenzel equation, leads to transition from the hydrophilic to
the superhydrophilic state. The attaining of highly roughened state
of our samples, obtained by laser texturing is also confirmed by the
extremely large values of water contact angle on the same surfaces
after modification by fluorooxysilane (Table 1). An axial symmetry Fig. 4. The time evolution of surface tension in the droplets of water (circles),
of the sessile water droplets on such superhydrophobic surfaces dispersions of E. coli (stars), and bacteriophage EcD7 (diamonds) at prolonged
indicates isotropic wetting with respect to deionized water. contact of the droplet with the superhydrophobic AMG alloy substrate.

The wettability results presented in Table 1 for chemically mod-

ified substrates indicate the heterogeneous wetting regime and the
superhydrophobic state with respect to water, as well as to
dispersions of E. coli and EcD7 at a titer of 1  107 CFU (PFU)/mL.
Corresponding data on the bacteriophage dispersions at a titer of
1  108 and 1  109 PFU/mL are presented in Table S1 in the
Supporting Information. Since the peculiarities of a liquid droplet
spreading are affected by the liquid/vapor surface tension, we
studied the evolution of the surface tension of a droplet of water
and biologically relevant dispersions versus time of contact with
the substrate. Decreased initial value and a sharp deterioration of
the surface tension for both the bacterial and the bacteriophage
dispersions just after droplet deposition, shown in Fig. 4, unam-
biguously indicate the surface activity with respect to water/vapor
interface of both studied dispersions. The decrease in the magni-
tude of surface tension for both dispersions is related to
diffusion-limited transport of biological species to the surface
and appear due to the presence of hydrophobic moieties both in
outer protein shells in the bacteriophage and the outer membrane
and lipopolysaccharide layer of E. coli.
3.3. Analysis of spreading
The analysis of the rheological properties of biologically
relevant liquids should take into account that the dispersions of
bacteria or bacteriophage demonstrate, in some cases, coordinated
motions [49,50] on length scales comparable or larger the charac-
teristic sizes of a biological object and resulting in non-Newtonian
behavior [51,52]. For example, the E. coli cells perform run-and-
tumble motion using a propulsion apparatus consisting of a collec-
tion of flagella [53,54], whereas the bacteriophage as an immotile
virus exploits the rotation of the bacterial flagella in order to pas-
sively travel along it and to reach the cell body for infection [50]. In
this study, to characterize the rheological properties of studied liq-
uids, the measurements of the dynamic viscosity at shear rate of
980 s1 were performed at T = 25 °C and the results are presented
in Table 1. Besides, we have shown the measured values of density,
initial values of surface tension and the pendant droplet radius for
water and biologically relevant dispersions.
The obtained data indicate very close values of both the density
and the dynamic viscosity for all three studied liquids. The spread-
ing kinetics of deionized water droplet on hydrophilic textured
AMG substrate is illustrated in Fig. 5. The spreading process starts
once the droplet suspended at the end of the needle contacts the
textured substrate. The snapshot of the top view of the spreading
droplet is shown in Fig. 5a, while in Fig. 5b the evolution in time
of the positions of three liquid spreading fronts discussed above
is presented.

Table 1
Physicochemical parameters of liquids studied in this work and the wettability of surfaces by these liquids.

Parameter Liquid
Deionized water Dispersion of bacteriophage EcD7 (107 PFU/mL) Dispersion of E. coli (107 CFU/mL)
3
Density, g/cm 0.99802 ± 0.00005 0.99800 ± 0.00002 1.00271 ± 0.00001
Dynamic viscosity, mPas 0.991 ± 0.001 0.993 ± 0.006 0.994 ± 0.003
Initial surface tension, mN/m 72.0 ± 0.1 64.6 ± 0.4 69.3 ± 0.3
Pendant droplet radius, m (1.1 ± 0.1)  103 (9.6 ± 1.0)  104 (9.6 ± 1.0)  104
Contact angle, °, on polished sapphire plate 81.4 ± 0.5 80.8 ± 1.0 72.8 ± 0.7
Roll-off angle on polished sapphire plate No rolling No rolling No rolling
Contact angle, °, on laser textured AMG2 substrate 172.3 ± 0.9 172.0 ± 0.3 172.3 ± 1.0
modified by fluorooxysilane
Roll-off angle, °, on laser textured AMG2 substrate 0.8 ± 0.4 1.1 ± 0.2 1.0 ± 0.3
modified by fluorooxysilane
 A.M. Emelyanenko et al. / Journal of Colloid and Interface Science 567 (2020) 224–234 229

Fig. 5. Spreading of water droplet atop of the textured AMG substrate. (a) Top view of the spreading droplet at an arbitrary instant and (b) time evolution of positions of
various spreading fronts. The points in (a) and lines in (b) shows positions of fronts associated with the propagation of liquid within the nanotextured features (1, 2), the
spreading along microchannels (3, 4) and the position of bulk droplet base (5, 6) along the fast (1, 3, 5) and slow (2, 4, 6) axes. The arrow in (a) indicates the direction of laser
scanning.

3.3.1. Spreading of droplet base
The spreading behavior indicates anisotropic spreading of the
droplet along the rough substrate with multimodal roughness
and the set of parallel microchannels and intercalated trenches.
The directions of fast and slow axes can be easily revealed from
the image of the elliptical liquid spot as the directions correspond-
ing to the highest and the lowest liquid spreading velocity, respec-
tively. It is interesting to note the anisotropy of the initial state of
the bulk water droplet base, spreading atop of liquid impregnated
textured surface in contrast to an isotropic decane droplet base
spreading atop of the same texture [39]. The analysis of the evolu-
tion of droplet shape has shown that for 6 lL droplets, no expan-
sion of bulk droplet base was detected along fast axis and only a
short time period of spreading along the slow axis after the droplet
was completely transferred to the substrate. However, faster
spreading along the fast axis had place once the droplet suspended
at the end of the needle contacted the textured substrate. This
conclusion follows from the elliptical shape of the droplet base just
after its transfer. This behavior shows to be typical for biologically
relevant liquids as well (Fig. 6).
3.3.2. Anisotropic spreading in the microchannels
Spreading of studied liquids in the microchannels was moni-
tored along both fast and slow axes and the kinetics of such
spreading is presented in Fig. 7. It is worth noting that the detailed
analysis of the substrate morphology (Fig. 3) indicates the smaller
sizes and meandrous configuration of microchannels/trenches ori-
ented along the slow axis of liquid spreading. In agreement with
the literature, for Newtonian liquids and diluted bacterial disper-
sion, the first stages of spreading along the microchannels are
described by Washburn type behavior. However, analysis of data
(Fig. 7) in coordinates Rm2 = f(t) indicates the existence of one linear
range for water and two ranges of linear dependences with differ-
ent slopes for dispersions of E. coli and EcD7. Such behavior of the

Fig. 6. The spreading of the drop base for droplets of water and biologically relevant fluids on the textured surface. The dimensionless radius was obtained by scaling the drop
base radius to the radius, a, of the pendant droplet before deposition on the surface; the dimensionless time was calculated as (tr/la), where t is time, r and l are the surface
tension and the dynamic viscosity of the liquid. (a) Spreading along fast axis; (b) spreading along slow axis. Dashed lines correspond to power-law fits with exponent
n = 0.101 ± 0.003. Inset in (a) compares the spreading behavior along two axes for the bacteriophage EcD7 dispersion droplet.
230 A.M. Emelyanenko et al. / Journal of Colloid and Interface Science 567 (2020) 224–234
Fig. 7. The spreading of liquid in micro-channels for droplets of water and biologically relevant fluids on the textured surface. (a) Spreading along the fast axis; (b) spreading
along the slow axis. Filled symbols indicate data points used for linear fits. Dashed and dotted lines are used to show the fits corresponding to the first and the second linear
ranges, respectively.
flows of biologically relevant liquids in the microchannels can be
explained by three factors. The first one is defined by the weakly
non-Newtonian rheology of the dispersions of both bacteriophage
and bacterial dispersions and is revealed through the variation of
the dispersion viscosity with a shear rate. A shear thickening
behavior at lower shear rates followed by a shear-thinning regime
at higher shear rates was observed earlier for the dilute E. coli dis-
persions [51]. It was shown that the viscosity maximum corre-
sponds to a shear rate on the order of the inverse of the time a
bacterium needs to swim over a distance of its own length [51].
The impact of bacterial motions on the flow of confined bacterial
dispersions was discussed in [55], where the rheology of dilute
E. coli dispersions under different degrees of confinement also
revealed a strong confinement effect. Thus, the viscosity of disper-
sion flowing in open microchannels should vary with the spreading
rate and across the channel.
The second factor is related to the surface activity of the biolog-
ical objects. As shown in Fig. 4, this surface activity results in the
temporal evolution of the liquid surface tension. Low depth of
the microchannels should lead to more efficient and rapid trans-
port of cells and viruses to the liquid/vapor interface and faster
decrease in surface tension with time than it was detected for
the sessile droplet (Fig. 4). Besides, smaller sizes of the transverse
channels lead to redistribution of the biological objects between
the flows in the microchannels along fast and slow axis. Thus, it
is expected that the system of microchannels acts as a kind of
membrane leading to the flow-induced redistribution of compo-
nents of biologically relevant liquid.
The third factor seems to be related to the redistribution of dis-
persion components between streams flowing along the longitudi-
nal and transverse channels. Such redistribution leads to an
increase in the concentration of particles (cells or viruses) in wider
Table 2
The slopes K of the dependences Rm2 = K(t  t0) for water and biologically relevant dispersions for the advancement of liquids along the microchannels.
Liquid Fast axis, mm2/s
Linear section 1
Deionized water 52
Dispersion of bacteriophage EcD7 68
Dispersion of E. coli 57
longitudinal channels along the direction of the fast spreading axis.
In contrast, the concentration of particles in the transverse chan-
nels is lower than the concentration in the bulk drop and in the
longitudinal channels. As a result of such redistribution, an osmotic
factor may arise, which significantly affects the velocity of the
microfronts.
The complex interplay between the variation in dynamic vis-
cosity of the non-Newtonian dispersions and the liquid surface
tension causes the revealing of two different linear ranges in
Washburn type dependences (Fig. 7) with the slopes, given in
Table 2. It is interesting to stress a nontrivial variation in the slopes
of linear sections of Washburn type dependence for dispersions of
bacteriophage and bacteria, presented in the table, when the slopes
in the first linear section for the fast axis are of higher value for
EcD7, whereas, the slopes in the slow axis are of lower value for
EcD7, compared to the values, obtained for the E. coli dispersion.
Such behavior is not completely clear at the moment. Presumably,
it may be due to the contribution of osmotic effects to the relative
movement of microfronts along the fast and slow axes.
3.3.3. Anisotropic nanopores impregnation
The increase in the area with nanopores impregnated by a liq-
uid causes eventual shrinkage of the bulk droplet base and
decrease in the radius of a liquid front in the microchannels. Very
narrow pores between nanoparticles forming the surface nanos-
tructures (Fig. 3b) initiate further separation of the components
of biologically relevant dispersion upon the advancement of the
nanofront. It is expected that in such a spreading process the pores
become filled with water rectified from the biological species. Such
a hypothesis correlates well with the fact that the laws of second
stage spreading of nanofronts in dimensionless coordinates for
water and biologically relevant liquid droplets (Fig. 8) are close
Slow axis, mm2/s
Linear section 2 Linear section 1 Linear section 2
49
32 43 11
27 48 14
 A.M. Emelyanenko et al. / Journal of Colloid and Interface Science 567 (2020) 224–234 231

a of the decane droplet spreading on top of the substrates with

10 Young contact angles varied from 0 to 15°, but with the same type
9
8
7 of texture, the data for the radius of fronts associated with the
6
5 E. coli impregnation of the nanotexture had shown the universal
Rn / a

4 EcD7 power-law Rn ~ t0.49±0.003. At the same time, the preexponential fac-

3 Water tors differed from each other and were dependent on the Young
2 contact angle. Recently a super-wetting situation, as a consequence
of surface roughness controlled wetting, described by the Wenzel
1 equation was considered by McHale et al. [56]. It was shown that
for such surfaces, the driving force for spreading of simple liquids
103 104 105 106
Dimensionless time depends on topography and chemistry and that such effect can sig-
nificantly affect the spreading exponent in Tanner law. In this
study, we deal with the spreading liquids characterized by Young
b
10
9
contact angle higher than 70° (see Table 1), which completely
8
7 wet the substrate according to the Wenzel law due to hierarchical
6
roughness of the substrate. Thus, the comparison of the nanofronts
Rn / a

5
4 spreading for decane and aqueous liquids allows concluding that
E. coli
3
EcD7
2 Water
1 According to the McHale’s model, the dynamic radius, Rn, of the
103 104 105 106
Dimensionless time
c of droplet axial symmetry and a lack of dynamic contact angle
Fig. 8. The imbibition of liquid into nanotexture for droplets of water and
biologically relevant fluids on the textured surface. (a) Along the fast axis; (b)
along the slow axis; (c) along the fast axis for 3 different concentrations of
bacteriophage EcD7. The dimensionless coordinates are the same as in Fig. 6.
to each other and are described by a power fit with an exponent of
n = 0.225 ± 0.004.
To check the universality in power fit description with the same
exponent for the dispersions in a wide concentration range we
have additionally analyzed the impregnation of the nanotexture
by bacteriophage EcD7 dispersions with the titer of 107, 108 and
109 PFU/mL. The obtained data shown in Fig. 8c in dimensionless
coordinates strongly confirms the validity of a power fit descrip-
tion with an exponent of n = 0.225 for all three concentrations.
Moreover, the almost complete coincidence of the dimensionless
the dynamics of surface structure impregnation can be tuned by
the peculiarities of the interaction between the liquid and the sur-
face texture.
front associated with the impregnation of the surface texture
depends on time as Rn ~ (t  to)1/(3p+1), where p varies from p = 3
in the case of flat and smooth substrate leading to the Tanner’s
law with spreading exponent n = 0.1, to p = 1 for rough surfaces,
when n tends to 1/4. However, as it was discussed in [56], the
derivation of the above equation for Rn is based on the assumptions
dependence entering into the cut-off for the viscous dissipation.
It is interesting to note that the analysis of the kinetics of water fill-
ing of the micropillar array covered by Si-incorporated diamond-
like carbon film treated by oxygen plasma in [24] detected the
dependence Rn ~ t0.25 for the wide time range. Data on the spread-
ing of water on superhydrophilic acrylate surfaces prepared by
photonic microfolding [57] also well correlated with the analysis
based on the McHale’s model with n = 0.23. In our experiments,
we deal with breaking of the assumption of droplet axial symme-
try. However, an attempt was made to analyze the nanofront
spreading using the above model [56] and basing on the hypothesis
that for all considered liquids we deal with the impregnation of the
nanotexture with water. According to the method proposed in [57]
and using the relation between the spreading velocity vn (vn = dRn/
dt) and the radius of nanofront Rn:
100
p=1.12 E. Coli
Water
p=0.95 EcD7
10
vn, mm/s

dependences of the nanofront radius on the impregnation time,

observed for solutions with concentrations differing by 2 orders
of magnitude, can also be considered as confirmation of the
hypothesis of impregnation of nanopores with a dispersion med-
ium purified from bacteriophage. It is interesting to note that the
dependences for the spreading of the bulk drop base (see Fig. S2
in the Supporting Information) for the dispersions of the bacterio- 1
phage with concentrations from 107 to 109 diverge significantly,
demonstrating an increase in the rate of spreading of the front with
the concentration increase.
2 3 4 5 6 7 8 9
There is a significant body of literature reporting that the 10
Rn, mm
advancement of liquid front penetrating the micro and nanotex-
ture follows a classical diffusion law of R ~ t1/2 similar to the Fig. 9. Representation of data on the impregnation of the nanotexture by water and
spreading of precursor wetting films. Indeed, in our recent study dispersions of E. coli and EcD7 in the frame of McHale’s model [56].
232 A.M. Emelyanenko et al. / Journal of Colloid and Interface Science 567 (2020) 224–234
logv n ¼ K  3p  logRn ;
the parameter p can be defined from the linear fit by plotting log vn
versus log Rn. Our experimental data plotted in the above coordi-
nates (Fig. 9) allowed getting p = 1.12 for the advancement of nano-
front for E. coli dispersion and p = 0.95 for both the bacteriophage
dispersion and water, leading to the spreading exponents of
n = 0.23 and n = 0.26, respectively. Having in mind the elliptic shape
of spreading nanofront and possible separation of dispersion com-
ponents by the texture elements, the above agreement between
the spreading exponents defined from Figs. 8 and 9 can be consid-
ered as satisfactory.
4. Conclusions
A bactericidal effect of many recently developed nanotextured
coatings is based on the fast spreading of biologically relevant dis-
persion along the surface with the uniform distribution of biologi-
cal organisms over the surface [4,6,58–60]. It is now well
established that cells respond to the nanoscale morphology of
the surfaces upon primary adhesion of the biological objects to
the surface. Contact interaction of cells with nanotexture is impor-
tant because it can induce the contact guidance, that is, the modi-
fication of cell morphology, orientation, motility and
differentiation [61–64]. The functioning of viruses, like bacterio-
phage, upon their seeding into nanotexture by spreading liquid
was poorly studied earlier. That is why the detailed analysis of
the spreading behavior of dispersions of bacterial cells or viruses
will lead to better operational conditions for achieving the desired
bactericidal effect. In this study, we have tested the hypothesis that
the distribution of biological objects upon spreading of biologically
relevant dispersions over laser textured surfaces is affected by the
substrate chemistry and roughness. The spreading of droplets of
water and dilute aqueous suspensions of bacterial cells of E. coli
strain and bacteriophage EcD7 over the superhydrophilic sub-
strates with multimodal surface roughness was studied experi-
mentally and compared with known theoretical predictions. For
that purpose, we have designed the hierarchically rough surfaces
using laser processing and have developed new techniques and
software based on digital image processing, which allow analyzing
the droplet spreading process in more detail, than it was available
in standard versions of optical monitoring of droplet spreading
[11,18–20]. It was found that in contrast to earlier studies of water
spreading over laser textured surface [20], the sensitivity of the
proposed digital method is high enough to distinguish 3 spreading
fronts simultaneously propagating along the substrates textured
by laser raster scanning. Namely, the movement of bulk droplet
base, the flow along the microchannels, and the nanotexture
impregnation were obtained in the same experiment. The aniso-
tropy of spreading for all types of liquid fronts was found for our
substrates. However, at the stages of receding of droplet base,
the bulk droplet acquired an axisymmetric shape. At the same
time, the elliptic shape was characteristic of the micro and nano-
fronts associated with the advancement of liquid along the
microchannels and the nanotexture impregnation. The highest
spreading velocity was found for the front associated with the
impregnation of nanotexture. Despite expected difference in the
rheological behavior of water and the biologically relevant liquids
related to non-Newtonian features of biologically relevant liquids,
which were discussed in the literature [51,52], the spreading
behavior of all tested liquids was successfully described by
power-law fits. Thus, the droplet base spreading along the slow
axis direction for all tested liquids followed the Tanner law
[7,9,23] with spreading exponent n = 0.1.
The advancing of water and dispersions in the microchannels
along both fast and slow axes was described by Washburn type
behavior [29,36,37]. However, in contrast to water, for biologically
relevant liquids two ranges of linear dependences of R2m on (t  t0)
was observed in the advancing stage, which is associated with the
time variation of surface tension for the dispersion, the depen-
dence of the dynamic viscosity on the velocity of front propagation,
and the flow-induced separation of components of dispersion in
confined channels. The analytical description of the front associ-
ated with the second stage of nanotexture impregnation for water
and biologically relevant liquids demonstrated universality in
power fit description in dimensionless coordinates with an expo-
nent n = 0.23 and well correlated with the analysis based on the
McHale’s model [56,57]. The flow-induced separation of compo-
nents of a biologically relevant dispersion observed here on the
basis of rheological behavior of spreading droplets of dispersion
may have a significant impact on the design of functional biointer-
faces. In future research, we plan to study the morphology and dis-
tribution of biological objects over the surfaces upon liquid
spreading and the cell response to the nanoscale morphology and
orientational ordering of fluid flow.
CRediT authorship contribution statement
A.M. Emelyanenko: Investigation, Writing - review & editing. L.
B. Boinovich: Conceptualization, Writing - original draft. K.A.
Emelyanenko: Software, Investigation.
Declaration of Competing Interest
The authors declare that they have no known competing finan-
cial interests or personal relationships that could have appeared
to influence the work reported in this paper.
Acknowledgments
The work was supported by the Russian Foundation for Basic
Research (grant # 18-29-05008), by the Ministry of Science and
Higher Education of the Russian Federation and by the Program
for fundamental studies of the Presidium of the Russian Academy
of Sciences. The authors wish to express their gratitude to Prof.
A.V. Aleshkin for providing the sterile phage lysate of the bacterio-
phage EcD7 and to Dr. A.G. Domantovsky for preparation of the
SEM images.
Appendix A. Supplementary material
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.jcis.2020.02.006.
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