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Review Article

Assembly of Heterogeneous Materials for Biology and Electronics: From Bio-Inspiration to Bio-Integration OPEN ACCESS

[+] Author and Article Information
Yuyan Gao

Department of Engineering Science
and Mechanics,
The Pennsylvania State University,
University Park, PA 16802

Huanyu Cheng

Department of Engineering Science
and Mechanics,
The Pennsylvania State University,
University Park, PA 16802;
Materials Research Institute,
The Pennsylvania State University,
University Park, PA 16802
e-mail: huanyu.cheng@psu.edu

1Corresponding author.

Contributed by the Electronic and Photonic Packaging Division of ASME for publication in the JOURNAL OF ELECTRONIC PACKAGING. Manuscript received December 1, 2016; final manuscript received February 22, 2017; published online June 13, 2017. Assoc. Editor: Xiaobing Luo.

J. Electron. Packag 139(2), 020801 (Jun 13, 2017) (16 pages) Paper No: EP-16-1131; doi: 10.1115/1.4036238 History: Received December 01, 2016; Revised February 22, 2017

Specific function or application in electronics often requires assembly of heterogeneous materials in a single system. Schemes to achieve such goals are of critical importance for applications ranging from the study in basic cell biology to multifunctional electronics for diagnostics/therapeutics. In this review article, we will first briefly introduce a few assembly techniques, such as microrobotic assembly, guided self-assembly, additive manufacturing, and transfer printing. Among various heterogeneous assembly techniques, transfer printing represents a simple yet versatile tool to integrate vastly different materials or structures in a single system. By utilizing such technique, traditionally challenging tasks have been enabled and they include novel experimental platforms for study of two-dimensional (2D) materials and cells, bio-integrated electronics such as stretchable and biodegradable devices, and three-dimensional (3D) assembly with advanced materials such as semiconductors.

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In the course of evolution, structures and materials in nature have developed exquisite strategies with exceptional selectivity and adaptability. Bio-inspiration has long been a motivation for scientists and engineers to develop novel design concepts and seek new paradigms for challenging problems [1,2]. Such bio-inspired approach requires identification, understanding, and qualification of the design principles in nature and their counterparts in engineering practice [3,4]. For instance, biological tissues (e.g., bone, nacre, tooth, shell, and wood) exhibit exceptional mechanical properties (e.g., stiffness, strength, toughness, interface properties, and elastic stability) and the underlying principles have been applied for the development of biomimicking synthetic materials/structures (Fig. 1(a)) [59]. Various microstructures in nature have also been exploited in the design of soft-bodied robotics with capabilities that permit adaptive and flexible interactions with unpredictable environment (Fig. 1(b)) [2,10,11], reversible and adaptive color changes for camouflage and distributed sensing/actuation (Fig. 1(c)) [1214], and multifunctional surfaces (Fig. 1(d)) [1518] for water repellency, low/directional adhesion, low drag, anisotropic wetting, self-sterilizing, and antifogging/icing/fouling/reflection.

Bio-integration is a topic of broad and increasing interest in the past few decades. Use of such scheme has been envisioned to be applicable to nearly every aspect in biomedicine (Fig. 1(e)) [19], with examples ranging from robotic exoskeletons [20] to rehabilitation [21] (Fig. 1(f)). However, biological tissues are soft and curved, whereas electronic devices are rigid and planar. Therefore, there is a significant mismatch in materials and forms between them. Flexible and stretchable bio-integrated devices represent a unique class of electronics that can address the mismatch between biology and electronics [22,23] (Fig. 1(g)). The use of stretchable materials represents a significant effort in the development of such electronics, as evidenced in several review articles [2426]. However, there is still a strong appeal to include inorganic semiconducting materials for high-performance electronics. The core idea of inorganic bio-integrated devices exploits the heterogeneous integration of rigid structures on a soft polymeric substrate to interface with the biological tissues.

Ideally, direct fabrication of devices on soft polymers would provide a solution for the long-lasting problem in bio-integration. The conventional semiconductor fabrication process is, however, not compatible with the polymer, particularly due to the high temperature required in the process. To address this challenge, the heterogeneous integration of high-performance electronics on soft polymers is achieved by use of various assembly techniques, including microrobotic assembly, guided self-assembly, additive manufacturing, and transfer printing. The demonstrated device platform includes sensors, actuators, power supplies, and wireless control modules.

In this review article, we will first review assembly techniques for heterogeneous materials integration in Sec. 2. Next, enabled by heterogeneous materials integration, we will discuss the recent developments of novel experimental platforms for study of two-dimensional (2D) materials and cells in Sec. 3, bio-integrated electronics in Sec. 4, and assembly of three-dimensional (3D) structures in Sec. 5. In Sec. 6, we will then present the challenges and future perspectives, followed by a concluding statement.

Integrated systems require precision control over spatial position and orientation at high throughput. Manipulating micro- or even nanostructures to meet such requirement is challenging due to their small dimensions, fragile mechanical properties, and tendency to aggregate or bond irreversibly to surfaces [27]. In order to assemble various components from heterogeneous materials into a single structure or device, several strategies such as microrobotic assembly, guided self-assembly, additive manufacturing, and transfer printing have been developed. In this section, we will first summarize the basic concepts of microrobotic assembly, guided self-assembly, and additive manufacturing in Sec. 2.1, and then introduce the technique of transfer printing techniques in Sec. 2.2.

Microrobotic Assembly, Guided Self-Assembly, and Additive Manufacturing.

Microrobotic assembly is widely used as a pick-and-place manufacturing tool in microelectromechanical systems [28,29]. In such scheme, bio-inspiration has a major influence, where microgrippers [30,31] are designed to imitate manual actions by humans for integration of heterogeneous components. When the scale goes down to microregime, issues such as different scaling effect, limited on-board power, and challenging microfabrication have to be addressed. Microrobots are commonly employed in a fluidic environment to reduce adhesion [32]. Other mechanisms have also been developed for microrobots to manipulate microstructures and cells [33] (Fig. 2(a)), including ferromagnetic microtransporters [34] and magnetic helical microswimmers [35] driven by external magnetic fields, and laser-induced bubble controlled by optothermally actuation [36].

Guided self-assembly uses external fields such as flow [37,38], electrical/magnetic forces [39,40], directional crystallization [41,42], temperature gradient [43,44], or relief structures [45] to direct the motion of nanomaterials. Langmuir–Blodgett technique is one notable example that monolayer of nanomaterials on the air–liquid interface can be organized into an ordered array through a compression force [37,46]. For noncontact heterogeneous assembly guided by electrical [47,48] and magnetic [49,50] forces, the process typically occurs in a fluidic environment for easy manipulation. In particular, micrometer-sized reinforcing particles coated with minimal concentrations of superparamagnetic nanoparticles can be used in low magnetic fields to produce 3D orientation and distribution in composite structures [8,51]. Predefined rails may also be introduced in the microfluidic self-assembly process to transport microstructures along the rail toward an assembled structure [52,53].

As an emerging technique in advanced manufacturing, additive manufacturing [5457] creates a structure by forming successive layers of materials under computer control. With computer-aided design, structures of nearly any shape or geometry can be manufactured toward rapid prototyping. Although additive manufacturing is a versatile tool in building 3D structures [58] (Fig. 2(b)), multimaterial integration has been a challenge. For example, stereolithography exploits photopolymerization that uses light to link chains of molecules in the resin to build 3D structures in a layer-by-layer manner. Digital light projection is further introduced to project UV light through a 2D pattern to cure resin into the designed pattern, which is particularly useful for large-scale printing. But in order to accomplish multimaterial builds, special attention has to be given to the design of vat for easy removal and rinse of different photocrosslinkable solutions in projection stereolithography [59,60] or of crosslinking from multiple syringes but only at programmed locations [61] (Fig. 2(c)), both of which can be time-consuming. In a separate effort to address such challenge, 3D magnetic printing has been introduced to orient anisotropic reinforcing particles by magnetic fields during printing for heterogeneous composites [9]. As an alternative to stereolithography, inkjet printing is promising in heterogeneous assembly for tissue engineering and biocompatible scaffolds [6264]. The core idea of heterogeneous integration in inkjet printing exploits multiple nozzles for different materials at different locations. A new dimension such as control from magnetic field can also be added to the inkjet printing process. For example, applying low magnetic fields on deposited inks preloaded with magnetized stiff platelets can control the orientation of anisotropic particles that are used as building blocks [65,66] (Fig. 2(d)). In addition, other additive manufacturing techniques such as laser sintering [67], fused deposition modeling [6870], direct laser writing [71], and screen printing [72,73] can be reconfigured for heterogeneous integration.

Transfer Printing.

In heterogeneous integration, the technique of transfer printing is commonly explored to pick each material component from the growth substrate via a stamp and then to deliver it onto the target of interest. Transfer printing is a two-step process: pickup and printing, both of which can be programmed into a deterministic manner for material assembly and micro-/nanodevice fabrication [7477]. The pickup step refers to the retrieval of material or structure (termed as “inks”) from the growth substrate onto the elastomeric stamp; the printing step delivers the retrieved inks onto the target substrate [78] (Fig. 3(a)). The success of transfer printing in both steps relies on the competition of delamination at different interfaces. Therefore, control of interfacial adhesion plays a critical role in the design of transfer printing. A stronger adhesion at the stamp/ink interface than that of the device/growth substrate leads to successful pickup. An even stronger adhesion at the device/target substrate interface is required to release the device onto the target substrate. Without adhesive or adhesion promoter at these interfaces, the adhesion comes from the van der Waals interaction, which is controlled by materials property and surface area in contact. In order to understand the separation at the interface for the two steps in transfer printing, the concept of interfacial crack is introduced. The delamination process at an interface can then be understood by the initiation and propagation of an interfacial crack. The crack tip energy release rate G characterizes the amount of energy due to formation of new surfaces and other dissipative processes. The Griffith criterion from fracture mechanics dictates that the interfacial crack would propagate when the crack tip energy release rate reaches a critical value Gcrit, the fracture toughness of the interface. The pickup and printing steps require Gcritstamp/ink>Gcritink/growth and Gcritstamp/ink<Gcritink/receiver, respectively. When a viscoelastic stamp is used, the critical energy release rate Gcritstamp/ink for the ink/stamp interface monotonically increases with the retraction velocity [79], thereby enabling success of transfer printing by using a high (or low) retraction velocity in the pickup (or printing) step [78,80].

In order to overcome the limitation in materials that can be transfer printed and the selection of target substrate, advanced techniques of transfer printing are introduced to improve the robustness and efficacy of the transfer printing process. As an excellent example from bio-inspiration, the design that emulates the adhesion organ on the gecko's foot has been applied to transfer printing [81] (Fig. 3(b)). For example, the pressure-induced change in microstructure at the interface can either enlarge or diminish the area of contact, thus modulating the interfacial adhesion [82]. To explore this idea, Kim et al. [83,84] introduced an array of microtip structures at the interface (Fig. 3(b)-V). Upon pressure, collapse of microtips enlarges the area of contact to increase the stamp/ink adhesion for pickup. Recovery of deformed microtips from viscoelasticity drastically reduces the stamp/ink adhesion for an easy printing. Shape memory polymers can also be used as the stamp to enable a temperature trigger for recovery of deformed microtips, with a stronger adhesion force due to significantly increased Young's modulus at a temperature below the glass transition temperature [85]. The active, programmable pressure control introduced in the above technique offers deterministic assembly in one transfer printing process [8688]. Another mechanism the gecko uses for control of directional adhesion (Fig. 3(b)-VI) [82,89] has also been explored: directional loading in shear-assisted transfer printing [9092] and directional structure in angled-stamp transfer printing [93]. Octopus also inspires the design of smart adhesive pads for transfer printing, by actuating temperature-responsive hydrogel muscles to reversibly adjust the internal space and thus the pressure (Fig. 3(c)) [94]. Other advanced transfer printing techniques include mechanical switchable surface [95], water-assisted transfer printing [96,97], pedestal-shaped stamp transfer printing [98], and laser-driven noncontact transfer printing [99,100].

Two-dimensional materials have gained a central focus since the exfoliation of graphene in 2004 [101]. The planar geometry of the stamp shape in transfer printing provides a natural interface to transfer ultrathin 2D materials such as graphene and single-layered transition-metal dichalcogenides (TMDCs). The unique feature of heterogeneous assembly also allows integration of cells on experimental platforms for the study in basic cell biology.

Two-Dimensional Materials.

Unique electronic and optoelectronic properties of 2D materials are often induced in their synthesis and assembly processes. Specific function or application also requires integration of 2D materials in a heterostructure. As the attractive feature of 2D materials comes from the ultrahigh-specific surface area that enables sensitive energy band structure to perturbations, the transfer process plays a critical role in minimizing damages and controlling the interface property with other assembled layers. For example, chemical vapor deposition is widely used to synthesize large-scale, high-quality 2D materials such as graphene. To integrate graphene in a heterostructure, transfer printing provides a relatively simple yet high-fidelity means [102] to transfer graphene from its growth substrate (i.e., Cu) onto soft [103], perforated [104], or even step [105] surfaces (Fig. 4(a)). In particular, integrating graphene on a patterned or deformable substrate provides a unique method to induce strain or deformation in 2D materials. With a deformation resulted from the interfacial force between 2D materials and the substrate, the band gap of 2D materials can be altered [106].

Continuous efforts in the past few decades on the development of silicon-based electronics push the limit of Moore's law [107]. Heterogeneous integration of compound III–V semiconductors (e.g., InAs, AlxGa1-xSb, and InGaSb) on Si substrates has been actively studied due to their high carrier mobility and other optical, mechanical properties. To address the conventional limitations of growth of multilayers on Si, epitaxial transfer via the technique of transfer printing has been demonstrated for compound semiconductors on insulator layers (XOI) [108]. However, carrier mobility in III–V XOI degrades as thinning down [109]. TMDCs at single layer (∼0.7 nm) represents an opportunity for such challenge, and excellent transport property has been demonstrated by lowering the contact resistance [110,111]. In these studies, transfer printing serves as a key step in building XOI platforms [108] (Fig. 4(b)) for investigation of III–V semiconductors (enhanced electronic mobility, strain engineering, and quantum confinement [108,112,113]) and dichalcogenide heterostructures (high field-effect mobility, high photovoltaic responses, reduced extrinsic scattering, and novel thermoelectric generator [114117]). In particular, a van der Waals heterostructure device platform has been developed to fully encapsulate MoS2 within hexagonal boron nitride (hBN) for reduced extrinsic scattering, thereby significantly increasing the low-temperature mobility of MoS2 (Fig. 4(c)) [115].

Cells.

The heterogeneous assembly technique also creates powerful experimental tools for the cell study [118]. Living cell microarrays [119,120] provide a highly efficient cellular system for the investigation of cellular physiology, cytotoxicity, and drug screening. Taken together with the recent development in microfluidics, lab-on-a-chip platforms [121,122] have also been developed for culture of living cells and single-cell manipulation [123]. An alternative format takes 3D constructs such as cell spheroids and cells encapsulated in hydrogel [124]. An in-depth discussion on heterogeneous 3D assembly is provided in Sec. 5. Combining these platforms with electronics further opens new opportunities in basic cell biology, stem cell research, tissue engineering, and drug discovery/delivery.

Transfer printing or microcontact printing [76] is a versatile tool to transfer cells when biocompatible materials such as PDMS or hydrogel are explored for the stamp. For instance, directional and patterned cells growth can be controlled on patterned stamp [125,126]. In such study, special attention should be given to surface treatment and materials selection for different types of cells that need to be transferred and a detailed review of such consideration can be found in Ref. [127]. Integrating this idea with microwell cell culture arrays [128,129], biosensors [130], and drug delivery sheets [131] yields a potential multifunctional cell-culture platform that organizes patterned cells, measures real-time physiological signals, tests platform for new drugs, and in vivo transfer prints cell layers for therapy (Fig. 5) [132].

Heterogeneous materials integration allows assembly of inorganic electronic devices on soft substrates toward bio-integrated electronics. The examples range from simple sensors and actuators to complex integrated systems. The demonstrated sensors are capable of monitoring temperature [133], deformation [134], hydration [134136], and electrophysiology [137139]. Integration of several sensors provides a multifunctional platform [140,141] for diagnostics and therapeutics. Extensive reviews on bio-integrated electronics have been provided in several review articles [142145]. Therefore, only a selection of the highlights will be briefly discussed here.

Bio-Integrated Electronics for Continuous Health Monitoring.

Bio-integrated electronics are designed to be flexible and stretchable to not only conform to the complex geometry of the biological tissues but also deform with the natural motion from the biological processes. Ultrathin geometry in the structure provides flexible characteristic, as the bending stiffness scales with the cubic of its thickness. The maximum strain that may cause fracture in the structure also decreases linearly with the thickness. The linearly reduced energy release rate with thickness also results in robust bonding to the other layers in heterogeneous integration [146]. The stretchability of inorganic materials comes from structural design. The stretchable structures explore some of the following representative strategies: (1) expandable wires or springs, (2) prestrain to induce initial wavy geometry, and (3) island-bridge design to isolate deformation to wavy bridges. The core idea behind the island-bridge design exploits wavy metal interconnects to connect rigid device components anchored on the substrate. This robust design concept can be applied to nearly every sensor and integrated system.

Capable of deforming into nearly an arbitrary shape, bio-integrated electronics can conform to surfaces of the skin and internal organs. Without drastic curvature change in the surface of biological tissues, direct integration of such flexible and stretchable electronics provides a good interface to continuously monitor various vital signs for health monitoring. One representative example of epidermal electronics developed by Kim et al. [140] integrates sensors for monitoring of temperature, strain, and electrophysiological signals, as well as modules for power and data transmission (Fig. 6(a)). Capable of conformal contact with the texture of the targeted skin, the bio-integrated device integrated with piezoelectric elements enables in vivo measurements of soft tissue viscoelasticity in the near-surface regions of the epidermis, for both quasi-static and dynamic conditions (Fig. 6(b)) [147]. In addition to physical sensing, epidermal chemical sensing provides additional capability for physiological and security monitoring of chemical constituents (Fig. 6(c)) [148].

However, some biological tissues present surfaces with large variation in the curvature. Direct integration of interconnected devices on such surfaces would result in kinks, which can damage the device due to stress concentration or at least alter the function of the initial design. Strategic cuts in the interconnected devices, which fall into the Japanese paper cutting art of Kirigami, can be introduced to address this issue. In the 3D multifunctional integumentary membranes (3D-MIMs) designed for spatiotemporal cardiac measurements and stimulation (Fig. 6(d)), separate electric connections have been setup for various functional components primarily in one direction, allowing relative movements between functional components in the perpendicular direction [149]. The techniques in 3D shape identification and transfer printing of various functional components can be applied to the other 3D objects but limited to certain class of geometries.

The methods to design curvilinear electronics for precisely matching the 3D biological tissues are of particular interest. In order to integrate multifunctional devices on a complex 3D geometry, a stretchable mold of soft substrate from the geometry is first cast. Applying radial tension transforms it into a flat-shaped film on which device components connected by wavy metal wires would be mounted. The device can still be fabricated on a planar wafer, followed by transfer printing onto the flat-shaped film. Releasing the tension causes the mold to relax to its original shape, thereby providing a device with conformal contact to the complex 3D geometry [150152].

Transient Electronics.

Another recent development in transient electronics represents an important class of electronics that can address the specific need in temporary biomedical implants [153156]. By resorbing in the human body after a period of stable function for diagnostics/therapeutics, this emerging class of electronics obviates the need for recollection. The demonstrated transient electronics range from deep brain monitors for intracranial pressure and temperature [157] to spatiotemporal mapping of electrical activity from the cerebral cortex [158]. The requirement of dissolving every material component in the human body leads to the selection of bioresorbable materials in an ultrathin form to minimize the amount of material to be dissolved. The fact that the semiconductor-grade single-crystal Si undergoes hydrolysis [159] leads to a series of major developments. Taken together with transient metals (e.g., Mg, Zn, Fe) [160] for the conductor and metal oxide such as MgO (or SiO2) for dielectrics, Si-based high-performance transient electronics can be transfer printed on biodegradable polymer substrates (e.g., silk, poly(lactic-co-glycolic acid) (PLGA)) (Fig. 7(a)) [161].

As shown in this illustrative example, the selection of dissolvable materials in semiconductors, conductors, and insulators is critical in design of transient electronics. In addition to single-crystal Si, other inorganic semiconductor materials [162] (e.g., polycrystalline Si, amorphous Si, Ge, and an alloy of Si and Ge) as well as certain organic semiconductor materials (e.g., 5,5′-bis-(7-dodecyl-9H-fluoren-2-yl)-2,2′-bithiophene (DDFTTF) [163], indigo [164]) have also been demonstrated for high-performance electronics. As for conductors, metals are widely used due to their low resistance and high reliability, whereas conducting polymers have the potential to control the electric signal with ions and protons rather than electrons [165]. Lastly, insulators are important for both substrates and encapsulations. In order to provide a biocompatible interface to tissues, soft polymers including both synthetic materials such as poly(vinyl alcohol) (PVA) [163] and PLGA [166], and materials with natural origin such as silk [167] and gelatin [168], have been intensively studied. Direct device fabrication on such substrates presents significant challenge due to their low-processing temperature, thereby leading to limited resolution in the device by the use of stencil masks. Introducing transfer printing in the fabrication process nicely addresses this challenge [161], such that the conventional fabricated device layer can be assembled on these soft substrates (Fig. 7(b)).

In order to provide a period of stable operation prior to functional degradation, an encapsulation layer that serves as a barrier against solution molecule penetration has been introduced to protect the device [159,169]. However, a single layer for encapsulation is not an effective means due to uncontrolled defects. To mitigate this effect, an engineering solution has been developed to exploit multilayer structure for the encapsulation layer. The multilayer encapsulation layer can be constructed with either the same material such as multiple silk/air pockets [170] or different materials such as alternating SiO2/Si3N4 layers [169]. The lifetime of the transient device can be significantly extended due to the effect of cooperative elimination of leakage pathway.

Formation of 3D functional structures has long been an interest for nearly every micro-/nano-system, including energy storage [171,172], microelectromechanical components [173], and biomedical devices [174,175]. Methods based on residual stress-induced bending are naturally compatible with modern planar technologies. However, such schemes provide access to only certain classes of geometries, through either rotations of rigid plates or rolling motions of flexible films [176,177]. In addition, other methods such as volumetric optical exposures [178], fluidic self-assembly [179], or templated growth [180] can only be used to realize certain classes of structures in certain types of materials. As this mini review focuses on material/structure heterogeneous integration for high-performance electronics, we will briefly summarize the techniques that are capable of forming 3D structures from multiple materials particularly including semiconductors.

Layer-by-Layer and Direct Imprinting.

As shown in the cardiac sock discussed in Sec. 4.1, stacking multiple functional 2D components in a layer-by-layer manner results in multifunctional systems. Demonstrated examples range from bio-integrated devices [149] to optoelectronics and optogenetics [181]. In addition, the same concept of layer-by-layer manufacturing can be applied to 3D microfabrication. Analogous to masonry in construction sites, each layer in the 3D system is first prepared in microfabrication, followed by assembly via the technique of transfer printing [182,183]. Binding of assembled structure such as high-temperature annealing completes the fabrication. In comparison to conventional bulk micromachining, this manufacturing strategy provides an effective and fault tolerant means to construct complex 3D Si-based structures, including microelectromechanical systems comb-drive [184], micromirror [185], and metamaterials and metadevices (Fig. 8(a)) [186]. However, a large number of layers are required to have an accurate representation of the 3D structure, which can be time-consuming even with automated transfer printing tools.

Curvilinear Electronics.

In addition to applications in bio-integrated electronics, the idea of curvilinear electronics can also be applied to construct other 3D surface structures. The curvilinear concept in deformable lighting systems also opens wide applications, ranging from ergonomic designs in consumer electronics, to flexible display and photovoltaics, and to imaging devices for biomedical uses. For instance, stretchable GaAs photovoltaics assembled on elastomeric substrates with surface relief present simultaneous large areal coverage and high stretchability [187,188], due to strain isolation in the region of interconnects (Fig. 8(b)) [189]. Another recent development on microscale light-emitting diodes (LEDs) interconnected by wavy metal filaments in a mesh layout bonded on an elastomeric substrate provides a viable path for such system. Passive matrix addressing allows a programmed pattern of the LEDs to be lit for display/lighting (Fig. 8(c)) [190192].

Another illustrative example is eyeball-shaped digital cameras that were inspired the imaging systems in human and the animals. By integrating an imaging array on a hemispherical shape to mimic the design of human eyes, such eyeball-shaped camera with only simple components provides high-resolution imaging without aberration at the edge (Fig. 8(d)) [152]. Taking advantage of a hydraulic system to reversibly control the radius of curvature of the hemispherical shape on which the imaging array integrates, images at different focus distances can be collected (Fig. 8(e)) [193]. The arthropod compound eye is another beautifully designed imaging system in nature that features large field of view, high sensitive to motion, and infinite depth of field (Fig. 8(f)) [194]. Such bio-inspiration leads to the design of populating imaging elements on a hemispherical surface [195]. The hemispherical surface in this example is, however, generated from hydraulic actuation after integrating an array of imaging elements on the planar surface.

Guided Mechanical Assembly.

As an alternative to curvilinear electronics, guided mechanical assembly, inspired by the ancient Japanese paper folding art—origami, represents another direction for formation of 3D structures. Built on the “island-bridge” design that freestanding wavy interconnects deform out-of-plane into the third dimension upon mechanical stretching, other 2D patterns with selected bonding sites to the underlying soft substrate can also pop up into a 3D structure upon mechanical stretching or compression in the substrate. As shown in Fig. 9(a), Si nanoribbon in a serpentine shape with progressively increasing radii of curvature is first bonded at selected locations (marked by the red dots in the figure) to a prestretched polymeric substrate. Release of the prestretch then leads to the pop-up motion in the region that is only in weak contact with the substrate, resulting in a 3D helix [196].

When 2D patterns are changed from ribbons to membranes, strategic cuts have to be introduced in the design to release the strain, which would otherwise leads to strain concentration and fracture in the kink regions (Fig. 9(b)) [197]. The pop-up motion in the freestanding region between bonded sites comes from the design of thin ribbon with a small out-of-plane bending or twisting stiffness (wt3) in comparison to the in-plane bending stiffness (w3t), where w and t are the ribbon width and thickness, respectively. In addition, the bending or twisting curvature in each local region of the popped up structure is also controlled by its corresponding stiffness. Therefore, the spatial gradient in width and particularly thickness serves as an effective factor to control the sharpness of folding or crease (Fig. 9(c)), which is an important concept in origami. This strategy is demonstrated for origami assembly of 3D structures for materials from soft polymers to brittle inorganic semiconductors and length scales from nanometers to centimeters [198]. With a single layer of 2D patterns, the 3D structure that can be transformed is limited to open-layout geometry with a large hollow space inside. To address this issue, Yan et al. [199] explored multilayered 2D patterns via transfer printing to create a quantitatively different class of nested 3D structures, characterized by their large filling factors (Fig. 9(d)). Combining different strategies such as spatial thickness gradient and nested structure further creates a box-shaped structure that can be precisely actuated (Fig. 9(e)).

Future Perspectives.

As an accurate and high-yield approach for heterogeneous integration, transfer printing is well suited for high-volume manufacturing. For example, one study conducted by Gomez et al. [200] shows transfer performance is nearly not changed even after 30,000 print cycles or 300 h of operation. When residues of the stamp material such as PDMS are left on the transferred structures, it is desired to remove such residues for subsequent integration without attacking the underlying structure [201]. In addition, roll-to-roll printing method represents a suitable option for the large-scale manufacturing (Fig. 10(a)). Among various transfer printing techniques introduced in Sec. 2.2, the methods utilizing directional adhesion hold great promise as a pathway for roll-to-roll operation [202,203].

Although in vivo bio-integration is capable of addressing many challenging needs in diagnostics and/or therapeutics, the alternative of in vitro bio-integration also provides unique opportunities from basic cell biology study to drug testing. However, the study is limited by the traditional culture of the cells and such limitation may be overcome by the recent development in 3D bioprinting of tissues and organs (Fig. 10(b)) [204]. Other novel manufacturing strategies also open new opportunities for bio-integration. In an analogy to soft lithography, direct imprinting can transfer patterns from soft stamps to stiff substrates including Si. In addition to Si nanowire arrays [205], a variety of complex 3D patterns can also be created. The core idea of direct imprinting exploits the mechanism of metal-assisted chemical etching [206,207] that uses a prepatterned polymer stamp coated with a catalyst layer (e.g., noble metals) to etch target substrate materials (e.g., Si) submerged in an etchant solution (e.g., an HF-oxidizer solution). As this process relies on mass transport of reactants and products, traditionally challenging porous Si surprisingly facilitates the patterning to result in sub-20 nm resolution (Fig. 10(c)) [208]. However, the nonporous Si does not take the shape of the stamp due to diffusion block in the Si substrate. To overcome this challenge, the noble metal catalyst coating needs to be made porous to facilitate the mass transport. This method can also be used to pattern metals [209] or III–V semiconductors [210,211]. But once again, any single method may not be sufficient to build complicated heterogeneous 3D systems of an increasing demand, and opportunities exist when taking advantages of different approaches.

Given the rapid recent development in heterogeneous integration and bio-integration, an increasing number of small and big companies have also started to commercialize the bio-integrated electronics. On a viable path to the successful implementation, more in-depth studies are required for robust encapsulation or packaging strategies to ensure mechanical and electrical properties as well as minimal interference to the biological tissues. This is particularly important for biodegradable electronics that may be envisioned for long-term uses. Encapsulation also facilitates sterilization and cleaning for reuse. Therefore, packaging strategies that can meet a variety of different requirements still represent significant interest in the research community. However, the issues and challenges discussed here are not exclusive. The collective intelligence from scientists across disciplines will contribute to a great success in addressing challenges from bio-inspiration to bio-integration.

Conclusions.

In an attempt to address the long-standing challenge of bio-integration, several strategies learned from nature have been applied to several design aspects of this engineering practice. In particular, this mini review first discusses various assembly techniques and particularly transfer printing for heterogeneous material/structure integration. This simple yet practical tool can be directly applied to construct platforms for the study of various materials, cells, as well as development of novel devices. As an alternative to the current trend of pushing smaller and more powerful electronics, the stretchable tattoo electronics capable of dissolving in the human body that have been built with the technique of transfer printing may present another direction for the future electronics. In addition, transfer printing can also serve as a versatile tool for assembling of heterogeneous 3D structures, which may open another important direction for the future development.

The work is partially supported by the start-up fund provided by the Engineering Science and Mechanics Department, College of Engineering, and Materials Research Institute at The Pennsylvania State University. The authors also acknowledge the support from NSFC (Grant Nos. 11572161 and 11272260), ASME Haythornthwaite Foundation Research Initiation Grant, and Dorothy Quiggle Career Development Professorship in Engineering at Penn State.

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Figures

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Fig. 1

A variety of demonstrations for bio-inspiration and bio-integration. (a) Nanostructured artificial nacre that is made from oriented, paralleled montmorillonite clay platelets (C) and polyelectrolytes (P), by cyclic repetition of the P-adsorption/rinsing/C-adsorption/rinsing process n times to yield the (P/C)n multilayers. Inset shows phase-contrast atomic-force microscopy (AFM) image of a (P/C)1 film on Si substrate. Reprinted with permission from Tang et al. [7]. Copyright 2003 by Nature Publishing Group. (b) A soft robot, actuated by a simple pneumatic valving system at low pressures (<10 psi), is capable of crawling and undulation gaits to navigate a difficult obstacle. Adapted with permission from Shepherd et al. [11]. Copyright 2011 by National Academy of Sciences. (c) Color shift in chameleons is achieved through active tuning of a lattice of guanine nanocrystals within two superposed layers of (superficial, S-; deep, D-) dermal iridophores (chameleonidae: I, Chamaeleo calyptratus; II, Rhampholeon spectrum; III, Kinyongia matschiei; scale bar of 500 nm). Reprinted with permission from Teyssier et al. [12]. Copyright 2015 by Nature Publishing Group. (d) Hydrophobic effect of the leg of the water strider is illustrated in (I) a maximal-depth dimple (4.38 ± 0.02 mm, side view) before piercing the water surface. Inset shows a contact angel of 167.6 ± 4.4 deg. Scanning electron microscope (SEM) images of a leg show (II) oriented microsetae and (III) fine nanoscale grooved structures on a seta. Scale bars: (II) 20 μm, (III) 200 nm. Reprinted with permission from Gao and Jiang [17]. Copyright 2004 by Nature Publishing Group. (e) Tactile sensor sheet tightly conforming to a model of the human upper jaw (scale bar of 1 cm). Reprinted with permission from Kaltenbrunner et al. [19]. Copyright 2013 by Nature Publishing Group. (f) Design and prototype of a bio-inspired active soft orthotic device. Reprinted with permission from Park et al. [21]. Copyright 2014 by IOP Publishing. (g) Fully integrated wearable sensor array on a subject's wrist for measurement and analysis of sweat metabolites, electrolytes, and skin temperature. Reprinted with permission from Gao et al. [23]. Copyright 2016 by Nature Publishing Group. (See figure online for color).

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Fig. 2

Microrobotic assembly, guided self-assembly, and additive manufacturing. (a) Microrobotic creation of a heterogeneous structure of copper cylinders (100 μm diameter) and polystyrene spheres (200 μm diameter) encased in poly(ethylene glycol) dimethacrylate (PEG) hydrogels. Inset shows the magnetic coil system that remotely controls microrobots. Reprinted with permission from Tasoglu et al. [33]. Copyright 2014 by Nature Publishing Group. (b) Schematic overview of printing patterned vascular architectures. Serving as a sacrificial scaffold, 3D printed interconnected carbohydrate glass lattice dissolves after it is encapsulated in extracellular matrices (ECMs) along with living cells, yielding a tissue construct with vascular network that matches the original lattice. Inset shows heterogeneous integration of 10T1/2 cells in the interstitial space of a fibrin gel and human umbilical vein endothelial cells (HUVECs) in the vascular network via a single lumenal injection (scale bar, 1 mm). Reprinted with permission from Miller et al. [58]. Copyright 2012 by Nature Publishing Group. (c) 3D printer setup that uses syringe tools to load different hydrogels, which are crosslinked during printing by a UV–LED array. Printing inside an autoclaved bag generates sterile scaffolds. Reprinted with permission from Hockaday et al. [61]. Copyright 2012 by IOP Publishing. (d) Multimaterial magnetically assisted 3D printing system for heterogeneous composite materials. (i) Direct ink-writing system consisting of multiple dispensers (I), a mixing unit (II), movable head and table (III), a magnet (IV), and a curing unit (V). (ii) Printed object with internal helicoidal staircase with a scale bar of 5 mm. Reprinted with permission from Kokkinis et al. [65]. Copyright 2015 by Nature Publishing Group. (See figure online for color).

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Fig. 3

Basics and advanced techniques of transfer printing. (a) Schematic illustration of the generic process to transfer print solid objects: I, aligning and retrieval of prepared microstructures with a stamp from a donor substrate; II, delivery of the microstructures from the stamp to receiving substrate. Reprinted with permission from Meitl et al. [78]. Copyright 2006 by Nature Publishing Group. (b) Hierarchical microstructure of gecko setae and its application in transfer printing. (I) Schematic of tokay gecko (Gekko gecko). (II–IV) SEMs of rows of setae from a toe (II), a single seta (III), and spatulae (IV). Reprinted with permission from Autumn et al. [81]. Copyright 2000 by Nature Publishing Group. (V) SEM image of elastomeric stamps in microtip designs to control the contact area by collapsing/recovering the four microtips. Reprinted with permission from Kim et al. [83]. Copyright 2010 by National Academy of Sciences. (VI) Directional dependent adhesion to control gripping and releasing. Reprinted with permission from Murphy et al. [89]. Copyright 2009 by John Wiley and Sons. (c) Octopus-inspired smart adhesive pad (I, scale bar of 1 mm) to switch adhesion by reversibly adjusting the internal space and thus the pressure (II), via the actuation of temperature-responsive hydrogel muscles (III; R, radial muscles; M, meridional muscles; C, circular muscles). Reprinted with permission from Lee et al. [94]. Copyright 2016 by John Wiley and Sons. (See figure online for color).

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Fig. 4

Platforms for study of 2D materials. (a) Schematic of the self-release layer (SRL) methodology in combination with a pick-and-place elastomer stamp transferring graphene, in which patterned graphene is first picked up by an elastomeric stamp coated with self-release layer, by etching of growth substrate, followed by removal of self-release layer to release graphene on destination substrate. Reprinted with permission from Song et al. [103]. Copyright 2013 by Nature Publishing Group. (b) Fabrication scheme for ultrathin InAs XOI, and AFM images. (I) A two-step epitaxial transfer process assembles two layers of perpendicularly oriented InAs nanoribbon arrays with 18- and 48-nm thicknesses on a Si/SiO2 substrate (AFM images). (II) Schematic procedure for the assembly of InAs compound semiconductor-on-insulator (XOI), where epitaxially grown, patterned single-crystal InAs nanoribbon arrays are transferred on Si/SiO2 substrates with an elastomeric polydimethylsiloxane (PDMS) slab, by selective wet etch of the underlying AlGaSb layer. Reprinted with permission from Ko et al. [108]. Copyright 2010 by Nature Publishing Group. (c) Schematic of the hexagonal boron nitride (hBN)-encapsulated MoS2 multiterminal device on van der Waals device structure platform for Hall mobility at low temperature (bottom: zoom-in cross-sectional schematic of the metal–graphene–MoS2 contact region). The exploded view shows the individual components in the heterostructure stack. Reprinted with permission from Cui et al. [115]. Copyright 2015 by Nature Publishing Group. (See figure online for color).

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Fig. 5

Design and key applications of a soft cell-culture platform. (a) Cell-culture platform includes top patterned graphene nanoribbons and bottom Au nanomembrane impedance/temperature sensors on a low-modulus PDMS sheet (serpentine-shaped Au electrodes in inset, and expanded view of each element at the bottom). (b) Four key applications of the cell-culture platform: (i) aligning C2C12 myoblasts, (ii) in situ monitoring of proliferation and differentiation, (iii) in vitro evaluating the effects of novel nanomaterials and drugs, and (iv) transfer printing cultured cell sheets onto target sites of animal models in vivo. (a)–(c) Reprinted with permission from Park et al. [129]. Copyright 2015 by American Chemical Society. (See figure online for color).

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Fig. 6

Bio-integrated electronics. (a) Image of a multifunctional epidermal electronic device that integrates antenna, LED, and strain/temperature/electrophysiology sensors, with physical properties matched to the epidermis. Manual mounting of these systems on the skin is directly analogous to that of a temporary transfer tattoo. Reprinted with permission from Kim et al. [140]. Copyright 2011 by The American Association for the Advancement of Science. (b) Exploded-view schematic illustration of the conformal piezoelectric system (top view in the lower-left inset and a cross-sectional view of actuators and sensors in the black dashed region) for clinical and experimental characterization of soft tissue biomechanics. Reprinted with permission from Dagdeviren et al. [147]. Copyright 2015 by Nature Publishing Group. (c) (Left) Protocol to prepare temporary transfer tattoo electrochemical sensors: a, screen printing patterned electrode (in red) on the release agent-coated (olive) base paper (orange); b, applying adhesive sheet (blue) with protective coating (maroon) to the printed electrochemical sensor; c, removing protective sheet (i) to apply the tattoo on the skin (green), followed by dabbing with water (ii) to remove release agent-coated base paper (iii), thereby exposing the adhered sensor pattern to the external environment for remote sensing. The routine in d is for physiological monitoring: removing paper (i) to apply the tattoo pattern on the skin (ii), followed by removing the protective coating (iii). (Right) Various sensor designs on human skin to be subsequently interfaced with a handheld three-electrode potentiostat via pressure contact or even a self-powered micropotentiostat for extended operation. Reprinted with permission from Windmiller et al. [148]. Copyright 2012 by Royal Society of Chemistry. (d) Images of a representative 3D multifunctional integumentary membrane (3D-MIMs) integrated on a Langendorff-perfused rabbit heart for spatiotemporal measurement and stimulation across the entire epicardial surface, with white arrows highlighting various functional sensors in this system (scale bars of 6 mm). Reprinted with permission from Xu et al. [149]. Copyright 2014 by Nature Publishing Group. (See figure online for color).

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Fig. 7

Bio-integrated transient electronics. (a) Image of a proof-of-concept device that integrates Mg resistor, Si diode, Mg/MgO inductor and capacitor, and Si/MgO/Mg transistor on a thin silk substrate. The time sequence images show the dissolution of this device in distilled (DI) water for the first 10 min. Adapted with permission from Hwang et al. [159]. Copyright 2012 by The American Association for the Advancement of Science. (b) Procedures that use the technique of transfer printing to fabricate transient electronic circuits (complementary metal-oxide-semiconductor, CMOS) on biodegradable substrates. Fabricated device on a Si carrier substrate (I) is released by dissolving the sacrificial PMMA layer in acetone (II). Retrieval of the released device with a PDMS stamp (III, image of the device on PDMS in the inset) allows removal of the bottom diluted PI (D-PI) layer by reactive ion etching. Transfer printing onto a biodegradable PLGA substrate (IV), followed by another reactive ion etching of the top D-PI layer, completes the process (V). Adapted with permission from Hwang et al. [161]. Copyright 2014 by John Wiley and Sons. (See figure online for color).

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Fig. 8

Layer-by-layer 3D assembly and curvilinear electronics of photovoltaics, LEDs, and hemispherical electronic cameras. (a) Schematic of layer-by-layer 3D heterogeneous integration of four layers of metamaterial on a Si membrane: “U” resonators twisted by 90 deg, gammadions, fishnet, and “I” beam. The size of one unit in this four by four array is ∼2.5 mm. Reprinted with permission from Lee et al. [186]. Copyright 2016 by Nature Publishing Group. (b) Curvilinear GaAs solar modules exploit elastomeric substrate with surface relief to confine strains at the locations of the interconnections and away from the devices, enabling high areal coverage and high level of stretchability. Reprinted with permission from Lee et al. [187]. Copyright 2011 by John Wiley and Sons. (c) Optical images of a deformed array of micro-inorganic LEDs (6 × 6) on the sharp tip of a pencil, with white arrows indicating the direction of stretching. Reprinted with permission from Kim et al. [191]. Copyright 2010 by Nature Publishing Group. (d) Photograph of a hemispherical electronic eye camera based on single-crystalline silicon optoelectronics. Integration with a transparent hemispherical cap with a simple, single-component image lens, such camera is capable of high-resolution imaging with low aberrations. Reprinted with permission from Ko et al. [152]. Copyright 2008 by Nature Publishing Group. (e) Schematic illustration of a hemispherical electronic eye camera with tunable lens (upper) and tunable detector (lower) modules. Fluid pressure is used to dynamically adjust the radii of curvature in both lens and detector sheet. Reprinted with permission from Jung et al. [193]. Copyright 2011 by National Academy of Sciences. (f) A digital camera taking the form of an apposition compound eye is elastically transformed from a planar layout on which they are fabricated to a hemispherical shape through hydraulic actuation. Reprinted with permission from Song et al. [195]. Copyright 2013 by National Academy of Sciences. (See figure online for color).

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Fig. 9

Mechanical guided assembly of 3D structures. (a) Finite element analysis shows the process to assemble 3D single-crystal Si conical helices from 2D filamentary serpentine ribbons bonded at selected points (red dots) to a prestretched slab of silicone elastomer. Relaxing the strain in the elastomer induces compressive forces, which lead to coordinated out-of-plane motions in the Si to form 3D structures (SEM images of an experimental result at the lower right inset). Reprinted with permission from Xu et al. [196]. Copyright 2015 by The American Association for the Advancement of Science. Representative examples that demonstrate deterministic assembly of 3D mesostructures by introducing (b) symmetric cuts (kirigami) along the circumferential directions in 2D nanomembranes (reprinted with permission from Zhang et al. [197]. Copyright 2015 by National Academy of Sciences), (c) spatial thickness gradient to create creases (gray color denotes the creases with reduced thickness) (reprinted with permission from Yan et al. [198]. Copyright 2016 by John Wiley and Sons), (d) releasable, multilayer 2D precursors to form a 3D trilayer nested Si cages (SEM image of the final configuration, colorized) (reprinted with permission from Yan et al. [199]. Copyright 2016 by The American Association for the Advancement of Science), and (e) combined use of spatial thickness gradient and nested structure to form a plastic structure in a closed box shape from biaxial prestrain in the substrate (reprinted with permission from Yan et al. [199]. Copyright 2016 by The American Association for the Advancement of Science). (See figure online for color).

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Fig. 10

Roll-to-roll manufacturing, 3D bioprinting, and direct imprinting. (a) Images of the roll-to-roll apparatus for transfer printing (top: side view, bottom: top view). Reprinted with permission from Jang et al. [202]. Copyright 2016 by AIP Publishing. (b) 3D interweaving of biology and electronics via additive manufacturing in a bionic ear created from functional materials such as biological (chondrocytes), structural (silicone), and electronic (AgNP infused silicone) in a 3D printer. Reprinted with permission from Mannoor et al. [62]. Copyright 2013 by American Chemical Society. (c) Metal-assisted chemical etching transforms the shape of the stamping onto porous Si with sub-20 nm resolution. Reprinted with permission from Azeredo et al. [208]. Copyright 2016 by John Wiley and Sons.

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