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Microfluidic Future serves as a portal to spread the news and developments in the field of microfluidics with the world.
There are numerous filters to separate particles in liquid based on their size, which can be enough to isolate them; however, particle shape can be more important, as it distinguishes healthy red blood cells from those affected by sickle-cell disease or malaria. Shape can also be used to determine what stage a cell is in of the cell cycle, which would benefit researchers looking for dividing cells. Recent research by Dino Di Carlo of UCLA looks to separate particles of differing aspect ratios continuously, using inertial fluid-dynamics. His work, “Continuous Inertial Focusing and Separation of Particles by Shape,” featured in Physical Review X reminds me of his previous work to use inertial fluid-dynamics to continuously filter particles according to size.... Read more »
Masaeli, M., Sollier, E., Amini, H., Mao, W., Camacho, K., Doshi, N., Mitragotri, S., Alexeev, A., & Di Carlo, D. (2012) Continuous Inertial Focusing and Separation of Particles by Shape. Physical Review X, 2(3). DOI: 10.1103/PhysRevX.2.031017
Di Carlo, D., Irimia, D., Tompkins, R., & Toner, M. (2007) Continuous inertial focusing, ordering, and separation of particles in microchannels. Proceedings of the National Academy of Sciences, 104(48), 18892-18897. DOI: 10.1073/pnas.0704958104
Sugaya, S., Yamada, M., & Seki, M. (2011) Observation of nonspherical particle behaviors for continuous shape-based separation using hydrodynamic filtration. Biomicrofluidics, 5(2), 24103. DOI: 10.1063/1.3580757
In an effort to model the complex processes occurring in human bodies, Donald Ingber has pioneered the development of ‘organs-on-chips,’ reproducing the lung and the gut on microfluidic devices. These systems allow researchers to replicate and study organs without the use of human test subjects. While this is one of the best options, there are too many variables to control, understand, and more importantly, manipulate. At the other end of the spectrum is an in vitro study with a cell line and few variables that hardly resemble the real environment. Researchers in Switzerland have developed their own gut-on-a-chip that imitates a human gastrointestinal tract called the Nutrichip. They hope to use this microfluidic device to study the immune-modulatory function of food (with a strong focus on dairy food). This work is detailed in the article “NutriChip: Nutrition Analysis Meets Microfluidics,” which appears in Lab on a Chip.... Read more »
Back when I was in sixth grade, I remember reading a little blurb in some science magazine at school that in the future we could receive shots via a method that would feel as soft as a banana peel. Although I’m now a champ at taking shots, it’s still not a bad idea. We’ve had transdermal patches (think nicotine and birth control) for some time now, but those release their medicine over a period of time. A syringe is capable of delivering a dose at once, and can take a biological sample too. Researchers from the University of Pisa have developed this ‘syringe of the future’ within ‘A minimally invasive microchip for transdermal injection/sampling applications’ in Lab on a Chip.... Read more »
Strambini LM, Longo A, Diligenti A, & Barillaro G. (2012) A minimally invasive microchip for transdermal injection/sampling applications. Lab on a chip, 12(18), 3370-9. PMID: 22773092
On Microfluidic Future I like reviewing advancements in therapeutic or diagnostic devices because I’m really drawn to those areas of research. Every once in a while, however, I take interest in research for the sake for knowledge, like the Root Chip. I recently came across an article from Dino Di Carlo of UCLA that describes a microfluidic device used to study cancer cells. The article, “Increased Asymmetric and Multi-Daughter Cell Division in Mechanically Confined Microenvironments” appeared in PLoS ONE, which is an open access journal (very cool!).... Read more »
Henry Tat Kwong Tse, Westbrook McConnell Weaver, & Dino Di Carlo. (2012) Increased Asymmetric and Multi-Daughter Cell Division in Mechanically Confined Microenvironments. PLoS ONE, 7(6). info:/
Cells are quite valuable, especially when used for regenerative research, diagnostics or research. But harvested cells do not come presorted and need to be separated from a heterogeneous mixture of cells. There are already numerous methods to sort cells according to biophysical properties such as size, density, morphology, and dielectric or magnetic susceptibility. Cell sorting based on labels can have a higher specificity, but introduces extra steps to add and remove labels, which can affect the phenotype of the cell. Rohit Karnik of MIT has developed a cell sorting method based on cell rolling. The continuous, label-free process is described in “Cell sorting by deterministic rolling” in Lab on a Chip.... Read more »
Microfluidic devices are able to process small volumes of liquid and are comprised of microscale components, but the devices themselves are not often small themselves. These labs-on-chips are often limited to lives in labs instead of the remote areas that could really benefit from their use. The limitation comes in the form of support equipment used to process or analyze assays that are expensive, bulky, energy consuming and/or require trained professional operators. Syringe pumps are often used in labs to drive liquids used in assays at specific flow rates and to ensure that the right volume is used. The need for complicated, external flow equipment was recently addressed by a group from Peking University. The group’s paper, “Squeeze-chip: a finger-controlled microfluidic flow network device and its application to biochemical assays” was recently featured on the cover of Lab on a Chip.... Read more »
Li, W., Chen, T., Chen, Z., Fei, P., Yu, Z., Pang, Y., & Huang, Y. (2012) Squeeze-chip: a finger-controlled microfluidic flow network device and its application to biochemical assays. Lab on a Chip, 12(9), 1587. DOI: 10.1039/C2LC40125H
A lot of excitement surrounding microfluidics has been about its promising use in diagnosis in low-resource settings. Many infectious diseases present in developing countries are manageable or treatable with available medications, but still account for 1/3 of deaths. In these areas, multiple diseases present similar symptoms, leading to misdiagnosis and thus incorrect treatment. Hundreds of blood-based microfluidic immunoassays are available for diagnostic purposes, but they’re not all created equally. They require varying levels of sample processing or analysis that prohibit their deployment in low-resource settings. Further, while some diseases may have similar symptoms, they might require different detection techniques, with varying sample volumes, reagents and processing time, making it difficult to detect multiple diseases within the same system. This is the focus of recent work from Paul Yager of University of Washington. In his Lab on a Chip paper, “Progress toward multiplexed sample-to-result detection in low resource settings using microfluidic immunoassay cards,” he and his colleagues develop a system to detect both Typhoid fever and malaria.... Read more »
Lafleur, L., Stevens, D., McKenzie, K., Ramachandran, S., Spicar-Mihalic, P., Singhal, M., Arjyal, A., Osborn, J., Kauffman, P., Yager, P.... (2012) Progress toward multiplexed sample-to-result detection in low resource settings using microfluidic immunoassay cards. Lab on a Chip, 12(6), 1119. DOI: 10.1039/C2LC20751F
Microfluidic Future is by no means an accurate representation of all the current, ongoing research in microfluidics. Nevertheless, the fact that you won’t be able to find any articles about assays relying on a biophysical marker isn’t too far off the reality in microfluidics. I suppose this is partly due to the incredible amount of previous work on molecular markers when high resolution control hadn’t been realized yet. Regardless, I was happy to come across an article about a microfluidic device that indicates sickle cell disease risk using the disease’s biophysical characteristics. The work “A Biophysical Indicator of Vaso-occusive Risk in Sickle Cell Disease” appeared in Science Translational Medicine this past February and is a result of ongoing sickle research by MIT and Harvard Medical School. My friend originally forwarded me an article about it on Medgadget, which you should also check out, along with the podcast it mentions.... Read more »
Wood DK, Soriano A, Mahadevan L, Higgins JM, & Bhatia SN. (2012) A Biophysical Indicator of Vaso-occlusive Risk in Sickle Cell Disease. Science Translational Medicine, 4(123), 1-8. PMID: 22378926
It’s not hard to see that a lot here at Microfluidic Future focuses on the medical applications of microfluidics, but that doesn’t mean that I’m not interested in other ways the technology can be used. I love to see novel applications of microfluidics because progress for anyone is progress for everyone. That brings me to today’s post on the RootChip. If the name isn’t a total give away, I recently came across an article that uses a microfluidic chip to study the roots of plants. In the article, “The RootChip: An Integrated Microfluidic Chip for Plant Science” by Stephen Quake and other researchers from Stanford University, a device is developed to study the roots of Arabidopsis thaliana.... Read more »
Grossmann, G., Guo, W., Ehrhardt, D., Frommer, W., Sit, R., Quake, S., & Meier, M. (2011) The RootChip: An Integrated Microfluidic Chip for Plant Science. THE PLANT CELL ONLINE, 23(12), 4234-4240. DOI: 10.1105/tpc.111.092577
What’s So Great About Oral Diagnostics?
Well, a lot of things, but let’s start with the basics. In order to use a microfluidic device, you need some type of fluid right? Sure if you had some powder or fine material you could suspend it in a fluid, but for simplicity sake, let’s look at fluids as our test material. If you wanted to run a health-related diagnostic, you only have so many bodily fluids available before you have to get creative and very invasive:
Out of all those fluids, blood (or serum) has been the preferred liquid. It is extremely rich in information and can expose a lot about a systemic condition or report on ailments located deep within the body. You have to filter it if you don’t want the blood cells in your sample, but it’s just a needle prick away. Other ‘fluids’ like mucus or saliva require a bit more work because of how thick and viscous they are, plus you need to filter out the debris floating around in your mouth. If blood is so great, why do we need anything else? Although blood is a great global fluid, sometimes you can get more detailed information by going closer to the source of the problem and choosing a more local fluid, but perhaps one of the greatest reasons is because the process to obtain the blood is still invasive. In the ideal microfluidics world of the future, we would need very small sample sizes and pin pricks wouldn’t be that bad. For now, spitting into a cup is still easier than and more enjoyable than getting stuck. Plus, exposed blood is always a health concern, and should definitely be avoided if possible.... Read more »
Giannobile, W., McDevitt, J., Niedbala, R., & Malamud, D. (2011) Translational and Clinical Applications of Salivary Diagnostics. Advances in Dental Research, 23(4), 375-380. DOI: 10.1177/0022034511420434
Biomimetics. I love that word. Well, probably not as much as microfluidics, but it’s a close second. If you’re unfamiliar with the word, it basically refers to design that mimics biology. Biological systems have evolved into finely tuned machines, why not mimic them in order to synthesize what we need? Biomimetics isn’t new, it’s been around in one form or another for a long time (my favorite instance is Velcro), but our capabilities are broadening as we are able to manufacture at smaller, micro and nano levels. If you want to learn more about this topic, you should check out the Biomimetic Microsystems Platform at the Wyss Institute. Today I’d like to share biomimetic microfluidic research that mimics the silk-spinning process of spiders from Korea University.... Read more »
Kang, E., Jeong, G., Choi, Y., Lee, K., Khademhosseini, A., & Lee, S. (2011) Digitally tunable physicochemical coding of material composition and topography in continuous microfibres. Nature Materials, 10(11), 877-883. DOI: 10.1038/nmat3108
How would you detect a heart attack? There are some symptoms that might tell you that you are very likely having a heart attack. Although you might feel pain in the chest, shortness of breath or other known physical symptoms, that doesn’t mean you in are actually having one. Conversely, you may not experience these symptoms but an attack is well on its way. In addition to painful symptoms, an electrocardiogram can be used to further indicate if you’re having a heart attack, but it also isn’t always accurate. But what if you could detect a heart attack by monitoring cardiac specific biomarkers in the blood or saliva? Those attempts are well underway.... Read more »
Du, N., Chou, J., Kulla, E., Floriano, P., Christodoulides, N., & McDevitt, J. (2011) A disposable bio-nano-chip using agarose beads for high performance immunoassays. Biosensors and Bioelectronics, 28(1), 251-256. DOI: 10.1016/j.bios.2011.07.027
Whether you’ve been learning about microfluidics here at Microfluidic Future or somewhere else, you’ve undoubtedly come across the elastomer poly(dimethylsiloxane) (PDMS). PDMS has radically changed the capabilities of microfluidics (and its price tag) since it was first brought into microfluidics by George Whitesides in 1998. PDMS has effectively replaced glass and silicon which were borrowed from existing micromachining industries. PDMS has great resolution and can contain sub-0.1 µm features. But how is PDMS used, and what makes it so great? Hopefully you’ll have these answers by the end of this post.... Read more »
McDonald, J., & Whitesides, G. (2002) Poly(dimethylsiloxane) as a Material for Fabricating Microfluidic Devices. Accounts of Chemical Research, 35(7), 491-499. DOI: 10.1021/ar010110q
Ovarian cancer is the fifth leading cause of cancer related mortality among women. Like many diseases, there is a stark difference in survival rates depending on detection times. When ovarian cancer is detected at stage I, there is a 90% 5 year survival rate. Compare that with the 33% 5 year survival rate when the ovarian cancer is detected in stage III and IV. This disease is unfortunately asymptomatic at early stages, drastically eliminating the odds of discovery with enough time to make a difference.... Read more »
Wang, S., Zhao, X., Khimji, I., Akbas, R., Qiu, W., Edwards, D., Cramer, D., Ye, B., & Demirci, U. (2011) Integration of cell phone imaging with microchip ELISA to detect ovarian cancer HE4 biomarker in urine at the point-of-care. Lab on a Chip, 11(20), 3411. DOI: 10.1039/C1LC20479C
Sepsis is a big killer here in the United States. I know that I don’t really think about that in a normal day, but it’s the truth, and we can’t ignore it. As of 2005, it was the 10th leading cause of death and was just one of two infectious conditions listed in the leading 15 causes of death. Sepsis develops in 750,000 Americans annually, and more than 210,000 die. (That’s a mortality rate of 28 %!) Sepsis not only kills, but it’s accountable for $16.7 billion in annual economic burden. You can see why we need to focus on sepsis, but what is it exactly? Well, sepsis is a response by our bodies to systemic microbial infections. A range of pathogens can cause this reaction, and there is still no clear answer for all the effects on the body that are attributed to sepsis. In general, sepsis is believed to be caused by an infectious agent that compromises the immune system, leaving it unable to properly clear microbes. Treatments for sepsis have included antibiotics, recombinant drugs, membrane blood filtration and blood transfusions. However, these therapies don’t work effectively enough, and many patients die. Hemofiltration and hemadsorption have also been used to clear the blood, but these techniques can also non-specifically remove blood proteins such as cytokines, which are necessary to fight infectious agents. Whole blood transfusions are able to remove the pathogens, but at the expense of the patient’s own immune components and cells that are needed to keep fighting the infection. With all this stacked against us, what are we to do? Turn to a microfluidic therapy I guess.... Read more »
Melamed, A., & Sorvillo, F. (2009) The burden of sepsis-associated mortality in the United States from 1999 to 2005: an analysis of multiple-cause-of-death data. Critical Care, 13(1). DOI: 10.1186/cc7733
You could say that valves in microfluidics (or microvalves) are like street lights that control traffic along microfluidic channels. But I’d say that they’re more like police barricades, stopping anyone they want, wherever they want. The sole purpose of microvalves is to control flow within a microfluidics device, allowing them to become very complex and more automated. Without microvalves, all reactions and mixing must occur in the same space, unless they were premixed elsewhere, which might just eliminate the advantage of microfluidics.... Read more »
Elizabeth Hulme, S., Shevkoplyas, S., & Whitesides, G. (2009) Incorporation of prefabricated screw, pneumatic, and solenoid valves into microfluidic devices. Lab on a Chip, 9(1), 79. DOI: 10.1039/b809673b
Hey, how’s your biotin? What? No it’s not an organic metal, maybe you call it B7? You’re probably fine, but have you been depressed, lethargic or losing your hair lately? Biotin is pretty important; it’s necessary for metabolism within our cells, so I make sure I never leave home without it. It’s rare for someone to have a biotin deficiency, but if you want to know your levels, give me a drop of your blood, and I’ll have an answer from you in 10 minutes. How? Oh just my self-powered integrated microfluidic blood analysis system (but I like to call it SIMBAS for short)...... Read more »
Dimov, I., Basabe-Desmonts, L., Garcia-Cordero, J., Ross, B., Ricco, A., & Lee, L. (2011) Stand-alone self-powered integrated microfluidic blood analysis system (SIMBAS). Lab on a Chip, 11(5), 845. DOI: 10.1039/C0LC00403K
Microfluidic chemostat used to study microbes
I don’t quite have the resources to poll the United States and the rest of the world, but if I did, this is what I’d ask:
Do you know what microfluidics is?
Can you explain it to me?
Do you currently use anything with this technology?
We may never know the results of the poll, but I think I'd hear "No" for most of them. Have no fear, because today you’re lucky enough to read my Beginner’s Guide to Microfluidics.
To start with...... Read more »
Cardiopulmonary BypassCardiopulmonary Bypass (source) More than 1,000 adult and 50 pediatric patients undergo a surgery involving cardiopulmonary bypass (CPB) each day in the United States. A CPB is used when performing surgery on the heart or lungs, leaving them unable to perform their normal functions. But CPB introduces a lot of foreign material to the body, creating adverse reactions. The CPB assembly, drugs and surgical processes can each have their own inflammatory effects. Induced inflammatory responses may include the release of pro-inflammatory cytokines, endothelial dysfunction and complement, neutrophil and platelet activation. Analyzing the patient’s blood during CPB is necessary to tie an inflammatory response to its origin in order to reduce a systemic inflammatory response syndrome (SIRS). But in order to monitor the patient’s status, at least three ml of blood must be drawn from the CPB system each time. This blood must then be centrifuged to access its plasma component (read more about replacing the centrifuge). Three ml of blood isn't needed to get an accurate reading, but it fits into the current operating procedures. This looks like the perfect opportunity to implement a microfluidic device to continuously filter small volumes of plasma from the CPB system to be analyzed, which is exactly what researchers from Rutgers University did.MicrofilterFilter membrane sandwiched between channels The article“Microfiltration platform for continuous blood plasma protein extraction from whole blood during cardiac surgery” by Jeffrey Zahn et al. is featured in the 2011 issue 17 of Lab on a Chip. The authors wanted to create a lab-on-a-chip component to filter plasma from CPB while collecting only 50-100 µl every 15 minutes, which could be used for the duration of a procedure which may last four hours. The proposed device is simple and features two microfluidic channels separated by a semipermeable membrane. In order to increase the filtration rate, the device features 32 channels in parallel. The authors chose to use a membrane with a 200 nm pore size, which allows plasma and proteins of interest to cross into the filter channel while stopping the 6-8 µm red blood cells (RBC). Even though the pores are sized so that only proteins and plasma can pass, that doesn’t mean that they’ll always be able to do so. Some proteins and cells naturally adhere to foreign objects, creating a clot. We don’t want this to happen to our membrane, which could become mostly or completely clogged. While our pore size allows proteins and plasma to pass through at a faster rate than smaller pores, it is more likely to ensnare a cell that can’t pass through. In order to prevent the membrane from clogging, we can introduce an anticoagulant, such as heparin. Anticoagulants like heparin prevent blood from clotting by disrupting a series of reactions that occur in blood (To learn more, check out this video on Coagulation Cascade from Johns Hopkins University). We normally don’t want anticoagulants in our blood because it would stop us from healing, but they are used in surgeries to diminish reactions to tools or processes. Instruments can be coated with heparin, which the authors did for the filtration device, so that heparin doesn’t have to be added system-wide. The blood’s hematocrit (Hct) also affects the need for an anticoagulant. Hct represents the percent of the blood volume that is occupied by RBC. The mathematical maximum value would be 1, which would mean that the blood was entirely composed of cells and there was no plasma, while 0 would indicate that there are no cells in the blood. Therefore a higher Hct would have a higher density of cells passing through the device and would need more anticoagulant. The final device by the authors was able to deliver cell-free plasma which made up 15% of the blood volume. The authors noted that although the plasma is cell-free, they needed to verify the extent of hemolysis. Hemolysis is simply the destruction of (RBC). We don’t want this happening to our filtered blood and need to make sure this isn’t the reason that no cells are entering our filtrate. I think that this is a simple, yet needed piece of equipment. It is basically a membrane separating two microfluidic streams. Although the channels are small, (the largest width is no greater than 600 µm) the channels across the membrane are different sizes so that they will still align when put together by our imperfect hands. The construction of parts of the device must be precise, but the device becomes more accessible if it does not need a robot to assemble it. This still needs another attachable point-of-care device to actually test the plasma, but this is promising.Reference:Aran, K., Fok, A., Sasso, L., Kamdar, N., Guan, Y., Sun, Q., Ündar, A., & Zahn, J. (2011). Microfiltration platform for continuous blood plasma protein extraction from whole blood during cardiac surgery Lab on a Chip, 11 (17) DOI: 10.1039/C1LC20080A... Read more »
Aran, K., Fok, A., Sasso, L., Kamdar, N., Guan, Y., Sun, Q., Ündar, A., & Zahn, J. (2011) Microfiltration platform for continuous blood plasma protein extraction from whole blood during cardiac surgery. Lab on a Chip, 11(17), 2858. DOI: 10.1039/C1LC20080A
CartilageOur bodies are pretty much amazing. We can get hurt, and our bodies will heal our cuts and bones (with the right support). But not everything heals so easily, like cartilage. The cartilage in our joints is called hyaline cartilage and can be damaged from trauma or diseases like osteoarthritis. The other cartilages like elastic cartilage (found in our ears and nose) and fibrocartilage (found on tendons and ligaments) are a bit of a different story. The hyaline cartilage found on the articular surfaces of our bones can't heal like other parts of our body because it doesn't contain any blood vessels. The blood vessels would normally provide the cells and proteins to the damaged tissue. So, without blood, the damaged tissue pretty much does, nothing. Enter tissue engineering.Cartilage EngineeringWhen faced with something that won't fix itself, our initial impulse is to replace it. That was our first reaction too, but we can't replace cartilage with just anything. It is a very complex and dynamic tissue. Ideally we would replace it with fresh cartilage, but it's not so easy to grow. The engineered cartilage must have a functional shape, achieve specific mechanical properties and not cause an immunogenic response when implanted in the body. In order to encourage cartilage cells (called chondrocytes) to form tissue in three dimensions instead of the two-dimensional bottom of a dish, tissue engineers have been developing scaffolds. Scaffolds have four desired traits:Highly porous with interconnected network for cell growth and transport of nutrients and metabolic waste
Biocompatible and bioresorbable so that it can be replaced by the tissue
Ideal surface for cell attachment and proliferation
Mimic cartilage mechanical properties
Choosing the right material is pretty important, but devising a way to create a porous 3D network is also vital. Cells can't be cut off from transport of nutrients and waste, even though it's crazy to believe that chondrocytes only make up 1% of the volume in cartilage. Researchers at National Taiwan University have developed a new method to build cartilage scaffolds using a polymer called alginate, which is a gum extracted from seaweed. It has been used previously in other scaffolds, but the main advance made by the researchers is how it is manipulated. Microfluidic-generated Scaffold
The work by Feng-Huei Lin et al. is entitled "A highly organized three-dimensional alginate scaffold for cartilage tissue engineering prepared by microfluidic technology" and appears in the October issue of Biomaterials. The authors have developed a novel microfluidic method for creating the alginate-based scaffold. As depicted in their figure, alginate droplets are formed around nitrogen gas. Their formation is highly controlled resulting in monodisperse droplets, which means that they're all (statistically) the same in size and shape. These droplets fall from the device into a solution containing calcium ions. The calcium ions (Ca2+) cause the alginate to form a gel. But before that happens, the droplets form a pretty honeycomb pattern. While this looks nice, it has a very important function. Remember when I said that scaffolds need to have interconnected networks? Well the monodisperse droplets are able to align so that they fit together perfectly, creating hexagonal patterns around each droplet. Once the droplets have gelated, a vacuum is applied which removes the air bubbles and connects the network.This technique has seen some promising results when looking at how the cells attach, proliferate and survive. But some forms of alginate have been known to cause immunogenic responses which would be unattractive. Any resulting engineered tissue would need to be mechanically tested, which was not performed in this study.Overall, this research was pretty interesting. It's obviously relevant to us humans, but it also excites me because it is a form of therapeutic microfluidics. As you can see from the rest of my posts, a lot of microfluidic technology is used in diagnostics. Both are equally important, but occur in different frequencies, so you can understand why this would have a place in my heart.References:
Hutmacher, D. (2000). Scaffolds in tissue engineering bone and cartilage Biomaterials, 21 (24), 2529-2543 DOI: 10.1016/S0142-9612(00)00121-6... Read more »
Hutmacher, D. (2000) Scaffolds in tissue engineering bone and cartilage. Biomaterials, 21(24), 2529-2543. DOI: 10.1016/S0142-9612(00)00121-6
Temenoff, J., & Mikos, A. (2000) Review: tissue engineering for regeneration of articular cartilage. Biomaterials, 21(5), 431-440. DOI: 10.1016/S0142-9612(99)00213-6
Wang, C., Yang, K., Lin, K., Liu, H., & Lin, F. (2011) A highly organized three-dimensional alginate scaffold for cartilage tissue engineering prepared by microfluidic technology. Biomaterials, 32(29), 7118-7126. DOI: 10.1016/j.biomaterials.2011.06.018
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