Capillarity-Enhanced Organ-Attachable Adhesive with Highly

Research Article Cite This: ACS Appl. Mater. Interfaces 2019, 11, 25674−25681

www.acsami.org

Capillarity-Enhanced Organ-Attachable Adhesive with Highly Drainable Wrinkled Octopus-Inspired Architectures Sangyul Baik,†,§ Heon Joon Lee,†,§ Da Wan Kim,† Hyeongho Min,‡ and Changhyun Pang*,†,‡ †

School of Chemical Engineering and ‡Department of SKKU Advanced Institute of Nanotechnology (SAINT), Sungkyunkwan University, Suwon, Gyeonggi-do 16419, Republic of Korea

Downloaded via UNIV FRANKFURT on July 26, 2019 at 03:09:20 (UTC). See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles.

S Supporting Information *

ABSTRACT: Mimicking the attachment of octopus suction cups has become appealing for the development of skin/organ adhesive patches capable of strong, reversible adhesion in dry and wet conditions. However, achieving high conformity against the three-dimensionally (3D) rough and curved surfaces of the human body remains an enduring challenge for further medical applications of wound protection, diagnosis, or therapeutics. Here, an adhesive patch inspired by the soft wrinkles of miniaturized 3D octopus suction cups is presented for high drainability and robust attachment against dry and wet human organs. Investigating the structural aspects of the wrinkles, a simple model is developed to maximize capillary interactions of the wrinkles against wet substrates. A layer of soft siloxane derivative is then transferred onto the wrinkles to enhance fixation against dry and sweaty skin as well as various wet organ surfaces. Our bioinspired patch offers opportunities for enhancing the versatility of adhesives for developing skin- and/or organ-attachable devices. KEYWORDS: adhesion, biomimetics, octopus, wrinkles, adhesive patch

■

INTRODUCTION

In recent years, the architectures of octopus suction cups have become highly attractive to understand their attachment to surfaces under water. The suction cup can be separated into two portions: the infundibulum above and the acetabulum below.12,13 Mimicking their structures, various skin adhesives have reported strong, reversible adhesion to human skin in dry or wet conditions.14,15 In particular, inspired by the protuberance within the sucker’s lower acetabulum, adhesive patches with domelike architectures have been developed for robust attachment in dry and wet conditions by enhanced suction effect.16,17 Despite their prospects in wound protection and biosignal detection, insufficient surface adaptability and easy discharge of suction limit their fixation on skin for long-term use. Further investigations on the anatomy of octopus suckers indicate a difference in elastic moduli between the acetabulum and the infundibulum. The infundibulum consists of a highly soft tissue, which enables the sucker to attach to surfaces of various roughness.18,19 Moreover, the network of grooves on the exterior rim not only permits low pressure to maximize the contact area for suction but also flows residual water out of its contact area to enhance its surface interaction.19,20 However, the adhesive mechanism of such wrinkles with maximized contact area and water drainage on a wet substrate remains recondite, whereas satisfying structural and material conditions to replicate such octopus-like architectures have rarely been demonstrated.

Investigating the adhesive phenomena of nano-/microscale hierarchical architectures on the surfaces of natural organisms has inspired developments in biocompatible adhesive materials for various medical applications such as adhesive patches for wound protection or skin-/organ-attachable electronics. Nonetheless, achieving adequate interactions with human skin remains an ongoing, fundamental challenge. This is because skin, the outermost organ of the human body, is rough, hairy, and usually wet by water, sweat, and other body fluids.1,2 Conventional cyanoacrylate glue adhesives are viable choices for skin attachment. However, their cytotoxicity, low air permeability, and contamination may cause damages and allergic symptoms, thus unfavorable to skin.3−5 For such reasons, various adhesives with biologically inspired patterns of skin architectures have become captivating for their capabilities of strong, reversible adhesion.2,6,7 Unfortunately, their van der Waals interactions are severely attenuated upon contact with water and thus inapplicable to rough surfaces within the human body.8 To overcome such drawbacks, adhesives with musselinspired catechols,9 nanoparticles,10 and hydrogels with a dissipative matrix have proven to be highly effective in wet conditions due to interactions between their chemical components and engaged tissue.11 Such interactions, however, cannot be applied repeatably and may leave damages, redness, or impurities on the applied biosurfaces. Therefore, adhesives capable of effectively managing water out of their contact area to establish strong, direct contact against various human organs in wet conditions are desperately needed. © 2019 American Chemical Society

Received: March 29, 2019 Accepted: June 28, 2019 Published: June 28, 2019 25674

DOI: 10.1021/acsami.9b05511 ACS Appl. Mater. Interfaces 2019, 11, 25674−25681

Research Article

ACS Applied Materials & Interfaces

Figure 1. Adhesive patch with protuberance and highly soft wrinkles inspired by the anatomy of an octopus suction cup. (a) Octopus tentacle with clusters of suction cups. The octopus suction cup contains a protuberance in its acetabular chamber and soft wrinkles on the infundibular rim (b). (i) Schematic illustration of the wet adhesion of the PIA-sw patch on rough and sweaty skin surface. (ii) PIA-sw with highly soft wrinkles and a suction chamber. (iii) Drainable wrinkles populated on the exterior rim of the PIA-sw’s. (c) Schematic illustration of the octopus-inspired patch with soft wrinkles applied to sweaty skin. (d) Photograph image of the PIA-sw patch. SEM image magnifies the arrays of soft wrinkles and protuberance. Inset shows a tilted cross-sectional image of the wrinkles.

(PIAs) using well-known fabrication methods of micromachining and replica-molding (see Methods and Figure S-1 under the Supporting Information).22,23 The geometries of the protuberance within microcavity arrays have been optimized for skin adhesion according to previous reports.23 The patch was then prestretched and exposed to UV/ozone to apply wrinkled structures on the exterior of the microcavities, followed by selective transfer of the highly soft, sticky, and biocompatible tuned PDMS (t-PDMS) on the surface of the wrinkles for enhanced biosurface conformability (see Methods and Figure S2 under the Supporting Information).21 Through such processes, we developed our octopus-inspired patch with arrays of PIAs and highly soft wrinkles to overcome wetness, roughness (∼1.9 nm−240 μm), and softness (elastic modulus E ∼ 140− 640 kPa) of human skin (Figure 1c).24,25 The patch is thin, flexible (area ∼ 5 × 5 cm2), and densely populated with protuberance (∼250 μm radius) in microcavities and wrinkle (∼23 μm wavelength and ∼8 μm amplitude) structures on the surface (∼100 suckers per cm2) as shown in Figure 1d. A tilted scanning electron microscope (SEM) image of the patch surface verified high integrity and fidelity of both protuberance and wrinkle microstructures (Figure 1d). Morphology and Adhesive Characteristics of the Wrinkled Octopus-Inspired Adhesive Architectures against Dry and Wet Substrates. We then investigated the structural features of the wrinkles on the surface of the PIAs as a function of applied prestrain in Figure 2a(i). Herein, the wavelength steadily decreases with applied prestrain, a behavior that agrees with previous, well-established studies.26,27 Yet, the changes in amplitude from increasing prestrain are relatively negligible. SEM images of the patch morphologies for each

Here, we present an adhesive patch with microstructure arrays of tiny wrinkles and protuberance, inspired by the anatomy of octopus suction cups. To optimize the geometry of the wrinkles depending on applied prestrain during UV/ozone exposure, we developed a simple model that investigates their capillary behaviors against a wet substrate. After inking with a tuned composition of poly(dimethylsiloxane) (PDMS), the wrinkles are biocompatible, highly soft, sticky, and reversibly deformable to enhance adhesion and conformity on dry and sweaty skin surfaces in both normal and peeling directions.21 We finally demonstrate high versatility of our bioinspired adhesive by attaching it onto even rougher and curvier surfaces of various wet porcine organs to shed light in potential applications of outer/inner organ-attachable wound dressings and devices with therapeutic and diagnostic purposes.

■

RESULTS AND DISCUSSION Fabrication of the Wrinkled Octopus-Inspired Adhesive Architectures. Figure 1a displays a suction cup located on the tentacles of an Octopus vulgaris. While its lower chamber contains a rigid protuberance, the infundibulum is arrayed with soft, tiny wrinkles. Inspired by all such features, we developed an adhesive patch with their microscale architectures to enhance the surface area during wet adhesion and drain water out of the contact interface (Figure 1b(i)). As shown in Figure 1b(ii), the octopus-inspired architecture consists of a suction cup chamber with a domelike artificial protuberance and highly soft wrinkles on its exterior rim. Upon attachment, the wrinkles conform onto the engaged substrate, and water molecules are drained out through grooves of the wrinkles (Figure 1b(iii)). We first prepared a patch with protuberance-inspired architectures 25675


Research Article


Figure 2. Morphology and adhesive characteristics of the octopus-inspired wrinkles. (a) (i) Wavelength and amplitude of the PDMS wrinkles depending on prestrain. (ii) SEM images of the wrinkles with varying wavelengths according to applied prestrain. (iii) Dry and (iv) underwater pull-off adhesion strengths of the PIA-w samples with varying wavelengths against silicon wafer. (b) (i) Fluorescence imaging of microstructures before and after applying preload for full compression, as well as behavior of liquids upon release of preload. (ii) Mechanism underlying the adhesion of the wrinkles against an underwater surface. (iii) Wavelength-dependent adhesion of the wrinkles against a silicon substrate in underwater condition. (c) Schematic illustration of the PIA-sw with highly soft wrinkles of optimal geometry, a rigid backbone, and a suction chamber. SEM images depict the morphologies of the PIA-sw and wrinkles after selective transfer of t-PDMS. (ii) Dry and (iii) underwater measurements of normal adhesion strengths for PIA-sw, PIA-w, and PIA patch samples against silicon wafer in dry and underwater conditions. (iv) Cyclic adhesion measurements of the PIA-sw patch against silicon wafer in dry and underwater conditions.

condition confirm changes in the wavelengths of the wrinkles depending on the applied prestrain (see Figures 2a(ii) and S-3). As shown in Figure 2a(iii,iv), the normal adhesion of the PIA with wrinkles (PIA-w) against silicon wafer remains similar with varying wavelengths in dry conditions, but steadily increases in underwater conditions up to ∼22.6 μm, from which both wavelength and adhesion strength are saturated. Such adhesive performances can be explained by two mechanisms: drainage of water molecules and enhanced capillary interactions of the wrinkles. As shown in Figure 2b(i), fluorescence imaging displays the behaviors of water molecules when the PIA-w’s are in contact with a wet glass substrate. During full compression, most of the water is pushed out of the patch interface or into the chambers of the microcavities. Upon release of the preload, water residual remains trapped inside the microscale grooves of the drainable wrinkles due to strong capillary interactions, thus sealing the wrinkles to also sustain the suction effect. This is due to the capillary behaviors of the molecules, which spontaneously drain water out, as well as the relative hydrophilicity of the UV-/ ozone-treated chamber (contact angle ∼ 76.1°; see Figure S-4a), which readily captures water to induce suction.16

We propose a methodological model underlying the adhesive interactions of the wrinkles against a substrate in underwater conditions. Although the enhancement of dry adhesion by the splitting of wrinkle contact has been well-established in previous studies,28,29 we take a similar approach for the increase in contact between the wrinkles and a wet surface. Total adhesive stress (σtotal) of the octopus-inspired adhesive can be calculated by the sum of suction stress (σs) and capillary interaction (σc): σtotal = σs + σc.30 Shown in Figure 2b(ii), σc is estimated by considering the geometry of the wrinkles, expressed as ij cos θ1 + cos θ2 yz zz + C γ σc = R eγ jjj e j h + RRMS zz k {

(1)

where γ is the surface tension of the water (∼0.072 J/m ), θ1 is the contact angle of the DI water on the substrate (silicon wafer; θ1 ∼ 65.3°), θ2 is the contact angle of the DI water on the wrinkle surface (θ2 ∼ 115.4°; see Figure S-4b,c), h is the height of the liquid film (∼3 μm), and RRMS is the root-mean-square roughness of the wrinkles (see Supporting Methods and Figure S-5 under the Supporting Information for detailed morphological information of the wrinkles). Re and Ce are defined as the 2

25676


Research Article


Figure 3. Attachment of the PIA-sw patch against dry and sweaty human skin. (a) Measurements of normal adhesion strengths for PIA-sw, PIA-s, PIAw, PIA, and flat samples against pigskin in (i) dry and (ii) sweaty conditions. (b) (i) Demonstration of pull-off adhesion against a human arm. (ii) Photograph of the human arm surface upon detachment of the PIA-sw patch. (c) Cyclic pull-off adhesion measurements of the PIA-sw patch in comparison with a 3 M medical tape for 100 cycles of attachment and detachment in (i) dry condition and (ii) sweaty condition. Herein, the green arrows represent adhesion measurements after a simple cleaning procedure of rinsing with water or scotch taping. (d) (i) Profiles of peeling energy for the adhesive samples against pigskin in dry and sweaty conditions. (ii) Measurements of peeling energy depending on peeling angles against dry and sweaty pigskins. Inset photographs show the experimental setups for peeling at varying angles using a custom-built equipment. (e) Photograph of the PIA-sw patch conformally attached to a human finger in bending motion.

of PIA-w’s per unit area (∼100 × 103 cm−2). Based on wellestablished studies, σs = Δmaxπr2n,23 where Δmax is the pressure difference between the ambient pressure and the pressure of the lower chamber within the protuberance. Hence, total underwater adhesion stress would then result ÅÄÅ ÑÉ Å A2 ÑÑ 8 σtotal = ΔPmaxπr 2n + ÅÅÅÅ1 + π 4· 2 ÑÑÑÑ ÅÅÇ 3 λ ÑÑÖ ÅÄÅ y i y ÅÅ 2 ÅÅ(a − πr 2n)γ jjj cos θ1 + cos θ2 zzz + (2πrn + 4azzzz·γ ] jj h + r zz ÅÅ z ÅÅÇ RMS k { {

effective region at which formation of capillary bridges is enhanced and the effective circumference at which surface tension is applied, respectively. Herein, Re = k·R and Ce = k·C, since Re and Ce are enhanced from their initial interacting regions (R) and circumference (C) by a factor of k. The ratio of the length of wrinkles (l) to that of a flat surface (l′), k, can also be expressed as k=l/l′. Then, k can be written as a function of 1/λ as follows 8 A2 i1y k jjj zzz = 1 + π 4· 2 3 λ kλ{

(2)

Combining eqs 1 and 2, capillary interactions induced by the wrinkles can be expressed as ÅÄÅ ÑÉÄÅ ij cos θ1 + cos θ2 yz ÅÅ 8 4 A2 ÑÑÑÅÅÅÅ 2 zz σc = ÅÅÅ1 + π · 2 ÑÑÑÅÅ(a − πr 2n)γ jjj j h + RRMS zz ÅÅÇ 3 λ ÑÑÖÅÅÅÇ k { zy + (2πrn + 4azzzz·γ ] (3) {

(4)

Based on our assumptions, total adhesive stress in underwater conditions, which depends on the wavelength of the wrinkles, is plotted in Figure 2b(iii) (see the Supporting Information for detailed derivation); this is well in agreement with the experimental data. With optimal wrinkle geometries for maximized adhesion, we transferred the thin, biocompatible t-PDMS layer on the surface of the wrinkles to enhance the adhesive capabilities of the wrinkles for dry and wet conditions by increase in surface energy.

where a is the dimension of the unit area (1 × 1 cm2) of the adhesive, r is the radius of the microcavities, and n is the number 25677


Research Article


Figure 4. Applications of the PIA-sw patch against various wet human organs. (a) Substrate samples of porcine (i) heart and (ii) liver to demonstrate organ adhesion. (b) Comparison of adhesive performances of the PIA-sw patch with PIA and flat samples against wet heart and liver surfaces in pull-off and peel-off directions. Pull-off adhesion is measured under optimized prestrain of 4 N/cm2. (c) (i) Schematic illustration of attaching the PIA-sw patch to a defect of a porcine heart to prevent hemorrhage. (ii) Attachment of the PIA-sw patch to a laceration on the ventricle walls of a porcine heart while distilled water flows from a blood vessel into the ventricles. (d) (i) Schematic illustration of the PIA-sw patch attached to the surface of a porcine liver. (ii) Pull-off adhesion of the PIA-sw patch against a porcine liver substrate. (iii-1) Immediate detachment of adhesive samples attached to a porcine liver during the water submersion test. (iii-2) Robust wet attachment on a porcine liver in underwater conditions.

of external preload. This maintains the suction effect, since enhanced van der Waals forces of the wrinkles against the substrate are greater than their restoring force. Meanwhile, for underwater conditions, the lower contact angle of the soft wrinkles yields greater capillary interactions than wrinkles without the t-PDMS layer (see Figure S-8). To test the durability of the wrinkles, repetitive measurements of normal adhesion up to 100 cycles of attachment−detachment were conducted against the silicon wafer in dry and underwater conditions (Figure 2c(iv)). We confirmed no decreases in its adhesion strength and no structural collapses via SEM image of the patch surface after 100 cycles of attachment−detachment (see inset of Figure 2c(iv)). The patch also showed negligible decreases in underwater adhesion depending on storage time (see Figure S-9).

Herein, the complete octopus-inspired microstructure, namely, the PIA with highly soft wrinkles (PIA-sw), can be separated into three portions: a suction chamber within the inner portion, a rigid polymeric backbone for the PIA-sw, and highly soft wrinkles at the top surfaces of the microcavities (Figure 2c(i)). The t-PDMS showed relatively low Young’s modulus (E ∼ 6−21 kPa) compared with other compositions of PDMS (E ∼ 300 kPa for 5 wt % and E ∼ 1200 kPa for 10 wt %; see Figure S-6); this enables high deformability of the soft wrinkles with the morphologies of their engaged substrates. Figure 2c shows the amplified adhesion strength PIA-sw patch in (ii) dry and (iii) underwater conditions compared with PIA-w and PIA samples. For dry conditions, the highly soft and sticky characteristics of the coated wrinkle layer amplify physical interactions even under low preloads.21 As shown in Figure S-7, the wrinkles spread and fully compress against dry substrates upon appliance and release 25678


Research Article

ACS Applied Materials & Interfaces Attachment of PIA-sw Patch against Dry and Sweaty Human Skin. We demonstrate adhesive capabilities of the PIAsw patch against skin surfaces in Figure 3. Adhesion measurements in normal and peeling directions were done on a pigskin graft (area ∼ 3 × 3 cm2) in dry (∼50% relative humidity) and sweaty conditions using the items of custom-built equipment at room temperature (see Supporting Methods and Figures S-10 and S-11 under the Supporting Information for details). First, the PIA-sw patch achieved high normal adhesion onto pigskin in dry conditions with applied preloads owing to the physical interactions of the protuberance and wrinkle microstructures (Figure 3a(i)). Herein, highly soft and sticky mechanical properties of the wrinkles enable the patch to easily conform with the rough topology of skin. Against sweaty pigskin, the PIAsw’s also demonstrated strong attachment, attributed not only to the suction effect of the protuberance but also to enhanced capillary behaviors and drainage of water molecules induced by the highly soft wrinkles (Figure 3a(ii)). With such, the PIA-sw patch displayed maximized normal adhesion strengths in both dry (∼3 N/cm2) and sweaty (∼1.3 N/cm2) conditions. Figure 3b(i) indicates that the PIA-sw patch adhered strongly against a human arm during detachment in the pull-off direction. Hardly any sticky residuals such as chemical contaminations, traces of dust particles, and other impurities were observed upon full detachment from the applied arm. Shown in Figure 3c(i) and (ii), our bioinspired patch achieved high repeatability against pigskin under 100 attachment−detachment cycles with facile cleaning processes before each measurement (see Figure S-12); this is superior to a conventional acrylic-based 3 M medical tape, which showed major loss in its adhesion strength after 5 cycles on dry pigskin and almost no adhesion on sweaty pigskin. Furthermore, the capillarity-enhanced PIA-sw patch displayed robust adhesion strength in the peeling direction in both dry and sweaty conditions (Figure 3d(i)). Herein, the soft and sticky properties of the wrinkles of the patch enhanced elongation of the microstructures via energy dissipation, thus delaying crack propagation in its peeling region during detachment. To understand the adhesive behavior of the PIAsw’s against various curvatures, samples were peeled from the pigskin graft (area ∼ 3 × 3 cm2) at varying angles (30, 60, and 90°) (Figure 3d(ii)). In these measurements, the PIA-sw patch showed greater peeling energy in both dry and sweaty conditions for smaller peeling angles.31 With such, the PIA-sw patch displayed maximized peeling energy in both dry (∼55 J/m2) and sweaty (∼35 J/m2) conditions peeling from 30°. As shown in Figure 3e, we then placed the PIA-sw patch onto the finger of a human to observe conformal attachment even under bending motions. Such performances are advantageous to nonpatterned PDMS patch or scotch tape, both of which lost their adaptability during motions of the finger (Figure S-14). Attachment of PIA-sw Patch against Various Wet Human Organs. The bioinspired adhesive patch may potentially be applied not only against dry and wet human skin but also against various wet organs such as the heart and liver (Figure 4a). Achieving fixation against heart and liver surfaces is generally known to be more difficult than fixation against skin due to their softness (E ∼ 25−200 kPa for heart; E ∼ 5−7 kPa for liver), irregular morphologies, and constant presence of body fluids.32−35 Furthermore, previously reported adhesives with only the octopus-inspired protuberance architectures (without wrinkles) hardly attained adherence to wet and rough organ surfaces like the liver due to low adaptability.16 Yet, as shown in Figure 4b, the capillarity-

enhanced PIA-sw patch displays relatively high normal adhesion strength against both porcine heart (

Capillarity-Enhanced Organ-Attachable Adhesive with Highly

Recommend Documents