Microfluidics: The future of microdissection TESE?

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1 Systems Biology in Reproductive Medicine ISSN: (Print) (Online) Journal homepage: Microfluidics: The future of microdissection TESE? Raheel Samuel, Odgerel Badamjav, Kristin E. Murphy, Darshan P. Patel, Jiyoung Son, Bruce K. Gale, Douglas T. Carrell & James M. Hotaling To cite this article: Raheel Samuel, Odgerel Badamjav, Kristin E. Murphy, Darshan P. Patel, Jiyoung Son, Bruce K. Gale, Douglas T. Carrell & James M. Hotaling (2016) Microfluidics: The future of microdissection TESE?, Systems Biology in Reproductive Medicine, 62:3, , DOI: / To link to this article: Published online: 22 Apr Submit your article to this journal Article views: 714 View related articles View Crossmark data Citing articles: 2 View citing articles Full Terms & Conditions of access and use can be found at

2 SYSTEMS BIOLOGY IN REPRODUCTIVE MEDICINE 2016, VOL. 62, NO. 3, REVIEW ARTICLE Microfluidics: The future of microdissection TESE? Raheel Samuel a,b, Odgerel Badamjav a, Kristin E. Murphy c, Darshan P. Patel d, Jiyoung Son e, Bruce K. Gale b, Douglas T. Carrell a,d, and James M. Hotaling a,d a Andrology and IVF Laboratories, University of Utah, Salt Lake City, Utah, USA; b Department of Mechanical Engineering, University of Utah, Salt Lake City, Utah, USA; c Huntsman Cancer Institute, University of Utah, Salt Lake City, Utah, USA; d Division of Urology, Department of Surgery, University of Utah, Salt Lake City, Utah, USA; e Department of Electrical & Computer Engineering, University of Utah, Salt Lake City, Utah, USA ABSTRACT Non-obstructive azoospermia (NOA) is a severe form of infertility accounting for 10% of infertile men. Microdissection testicular sperm extraction (microtese) includes a set of clinical protocols from which viable sperm are collected from patients (suffering from NOA), for intracytoplasmic sperm injection (ICSI). Clinical protocols associated with the processing of a microtese sample are inefficient and significantly reduce the success of obtaining a viable sperm population. In this review we highlight the sources of these inefficiencies and how these sources can possibly be removed by microfluidic technology and single-cell Raman spectroscopy. ARTICLE HISTORY Received 4 December 2015 Revised 8 February 2016 Accepted 10 February 2016 KEYWORDS IVF; microfluidics; microtese; sperm separation Introduction Approximately 15-20% of couples in industrialized countries fail to conceive after one year [Boivin et al. 2007], and male factor infertility, characterized by semen parameters that fall below the World Health Organization (WHO) [Cooper et al. 2010] cut-offs for normozoospermia, is thought to underlie nearly half of these cases [Brugh and Lipshultz 2004]. The most severe form of male infertility, non-obstructive azoospermia (NOA), is defined by the lack of sperm in the ejaculate and very little to no sperm production within the seminiferous tubules [Kumar 2013]. There are many potential causes for NOA, including genetic and congenital abnormalities, post-infectious issues, exposure to gonadotoxins, medications, varicocele, trauma, endocrine disorders, and idiopathic causes [Wosnitzer et al. 2014]. NOA accounts for approximately 10% of male infertility cases and is seen in around 1% of men in the general population [Krausz 2011]. With the development of in vitro fertilization (IVF) and intracytoplasmic sperm injection (ICSI), many otherwise infertile men have been able to successfully overcome barriers to conception, including NOA [Wang and Sauer 2006]. Because the sperm are in such low numbers in NOA patients (if any are present at all), identification and collection of these cells requires specifically-designed techniques in both the operating room and in the laboratory. The prevailing method used to collect testicular tissue for potential sperm recovery from NOA patients is by microdissection testicular sperm extraction (microtese). MicroTESE involves an open testicular biopsy under an operating microscope to selectively remove tubules that appear to have potential spermatogenesis, followed by tissue processing measures to isolate sperm and store sperm for subsequent use by ICSI [Schlegel 1999]. While the advent of microtese substantially improved sperm recovery compared to standard biopsy or other techniques [Deruyver et al. 2014], the procedure remains inefficient, costly, and very time consuming. The field of microfluidics provides interesting opportunities and has utility for many needs in cell biology, but is particularly powerful when considering applications in single cell or low cell number analyses [Sackmann et al. 2014]. Microfluidics is the science and technology of systems that process or manipulate small volumes (10 9 and liters) of fluids, using channels with dimensions of tens to hundreds of micrometers [Whitesides 2006, p. 368]. This unique technology has facilitated many important innovations, including some already found in the assisted reproductive technology (ART) field [Swain et al. 2013]. Because of the great need for improved efficiency and accuracy in processing the low cell counts involved in CONTACT James M. Hotaling jim.hotaling@hsc.utah.edu Andrology and IVF Laboratories, University of Utah, 675 Arapeen Drive, Suite 201, Salt Lake City, UT 84109, USA. Color versions of one or more of the figures in the article can be found online at Taylor & Francis

3 162 R. SAMUEL ET AL. microtese samples, the field of microfluidics may provide unique solutions to the varied problems currently encountered with the processing of microtese samples. While a number of microfluidic technologies have been previously developed for motile sperm separation, none have been implemented for microtese procedures. Currently, sperm detection and separation in samples with low sperm concentrations (microtese, oligozoospermic samples, etc.) is a time and laborintensive process. As a result, there is a great need for innovative approaches to improve the speed and efficiency of the process. Specifically, there are two key areas that may benefit from microfluidic technology, namely the identification of sperm in heterogeneous tissue preparations derived from TESE and microtese procedures, and the identification of high quality or genetically fit sperm in heterogeneous semen samples. This review summarizes and discusses the advantages and disadvantages of current microtese practices, focusing on potential novel laboratory sperm identification and isolation techniques using microfluidic technology. We examine and review microfluidic techniques that have demonstrated utility in current ART, and discuss novel microfluidic applications that may be applied to microtese to provide improvement in the efficiency and sensitivity of sperm recovery [Lenshof and Laurell 2010]. Sperm recovery via microtese With the development of ICSI [Palermo et al. 1992], the importance of testicular-derived sperm in treating obstructive azoospermia (OA) has rapidly become obvious [Craft et al. 1993; Silber et al. 1995; Schoysman et al. 1993]. To obtain testicular sperm, the use of a surgical testicular sperm extraction (TESE) method was employed, in which parenchymal tissue is harvested using an open testicular biopsy [Schlegel and Su 1997]. While the simple TESE technique has proved to be an effective means to retrieve sperm from patients with OA [Dohle et al. 1998], the technique was less successful in obtaining sperm from patients with NOA. Because spermatogenesis is often sporadic and isolated to rare seminiferous tubules in NOA patients, a non-selective tissue biopsy approach usually missed sites of sperm production, leading to poor sperm recovery [Schlegel and Su 1997]. These shortcomings led to a modification of the TESE procedure in 1996 in order to specifically suit cases of NOA. With the assistance of a high-powered operative microscope, it became possible to distinguish between seminiferous tubules without any germ cells, which appear smaller in diameter, and seminiferous tubules with focal spermatogenesis, which appear larger and more opaque. The resulting procedure, deemed microdissection testicular sperm extraction (microtese), allows for selective biopsy of tissues most likely to contain sperm, thus decreasing the amount of tissue removed and increasing the chance of sperm recovery [Schlegel 1999]. This method was found to be significantly more successful in retrieving sperm from NOA patients than simple TESE [Dabaja and Schlegel 2013; Deruyver et al. 2014; Tsujimura 2007]. Representative sperm retrieval rates increased from 16-45% using simple TESE to 42-63% using microtese [Deruyver et al. 2014]. Therefore, microtese surgery under 15-20x magnification is currently considered to be the leading option for obtaining sperm from NOA patients (Figure 1, box 1) [Dabaja and Schlegel 2013]. Tissue obtained by microtese requires careful processing in the laboratory in order to separate and identify sperm within the biopsied tissue. First, mechanical tissue-mincing methods are utilized in order to release spermatocytes from seminiferous tubules and eventually to achieve a tissue suspension. Various mechanical techniques are employed, including passing tissue through angiocaths/syringe needles, tissue shredding with fine needles or glass slides, tubule squeezing, or cell straining [Esteves and Varghese 2012; Popal and Nagy 2013]. Next, and most time-consuming, is the tissue-processing step which involves manually searching through the testicular tissue specimens for sperm. Testicular sperm are generally non-motile, making the search for sperm more difficult [Bettegowda and Wilkinson 2010]. Each microscopic field examined under x magnification contains a combination of red blood cells, white blood cells, sertoli cells, sperm precursor cells, and debris that must be distinguished from the spermatocytes [Esteves and Varghese 2012; Popal and Nagy 2013]. Depending on the level of spermatogenesis and the number of sperm cells present, this step may take as little as one hour to find a sufficient number of sperm, or as long as hours with multiple personnel examining tissue specimens to find just a handful of sperm [Ramasamy et al. 2011a] (Figure 1, box 2). Some clinics use an erythrocyte lysing buffer to reduce the number of red blood cells within the cell suspension, or pentoxyfylline to chemically induce in testicular sperm; however, these additives, like collagenase, are controversial for their effects on sperm viability [Popal and Nagy 2013]. Not only is manual microscopic testicular specimen examination time-consuming and tedious, it is also

4 SYSTEMS BIOLOGY IN REPRODUCTIVE MEDICINE 163 Figure 1. Flowchart depicting steps in typical microdissection testicular sperm extraction (microtese) procedure. The male partner undergoes a microsurgical testicular biopsy. Manual tissue processing and microscopic examination is carried out in order to identify sperm. Specimens containing sperm are cryopreserved in bulk. Prior to intracytoplasmic sperm injection (ICSI), frozen specimens are thawed and prepared for ICSI by density gradient centrifugation. Meanwhile, the female partner undergoes hormonal triggers and egg retrieval. If sperm are recovered, eggs are inseminated by ICSI. greatly dependent on personnel skill-level [Ramasamy et al. 2011b]. Sperm can easily be overlooked due to a number of variables including incomplete cell dissociation, elevated levels of other cell types, inexperience, exhaustion, or human-error. Furthermore, the longer a single person searches for sperm cells, the more errorprone they become [Ramasamy et al. 2011b]. For patients that produce a small number of sperm to begin with, failing to identify even a couple of sperm could mean the difference between infertility and a successful pregnancy. For these reasons, the sperm identification process is a crucial step of microtese. By removing the human-factor and moving towards automated and efficient cell separation, not only would it be possible for sperm to be identified faster and more accurately, but sperm could be separated from somatic cells and debris simultaneously, facilitating downstream preparation for ICSI. Predicting successful microtese sperm retrieval for any given patient is difficult, with the chances of identifying sperm at about 50% [Dabaja and Schlegel 2013]. Because the only route to fertilization using testicular derived sperm is via ICSI, sperm retrieval by microtese represents only half of the equation to achieve pregnancy for NOA patients. In preparation for ICSI, the female partner must undergo precisely timed hormonal triggers for weeks prior to oocyte retrieval (Figure 1). Thus, coordinating fresh oocytes simultaneously with microtese sperm retrieval has a major drawback; if no sperm are recovered from the male, the couple will have unnecessarily spent a great deal of time, effort, and money on ovarian stimulation and oocyte retrieval. Therefore, many clinics opt to cryopreserve sperm retrieved from microtese before retrieving eggs from the female partner [Ben-Yosef et al. 1999; Gangrade 2013; Tavukcuoglu et al. 2013; Oates et al. 1997]. This course of action, however, requires additional microtese processing steps. The ability to efficiently aliquot and cryopreserve small quantities of spermatozoa (minimum volume vitrification) sufficient for a single assisted reproduction cycle would benefit patients with limited quantities of sperm. Some laboratories use density gradient centrifugation to purge some of the unwanted somatic cells and to collect a more viable sperm population, yet this practice comes with the major drawback that sperm may be lost to the density gradient (Figure 1, box 4) [Oates et al. 1997]. Accordingly, the entire cryopreservation and thawing process could be optimized specifically for microtese cases in order to improve sperm recovery rates for ICSI. Development of a micro-scale cryopreservation system could allow sperm to be separated from somatic cells upon their identification, and then thawed without additional cell-processing steps. In summary, goals for improving microtese success in the near future should include increasing tissue processing consistency/efficiency, decreasing tissue processing time/cost, decreasing technician variability, and increasing cryopreservation consistency/efficiency. It is likely that such improvements can be made by the

5 164 R. SAMUEL ET AL. development of appropriate automated technologies that incorporate microfluidic systems for processing microtese samples. Current sperm selection techniques Conventional clinical sperm selection techniques such as morphology based selection methods, density gradient isolation methods, and physiological intracytoplasmic sperm injection (PICSI) method, have provided reliable solutions to isolate normal sperm from highly concentrated semen samples. Sperm morphology has long been known to be an important predictor of successful fertilization following conventional IVF. The morphology based selection generally occurs at 400x magnification, and ideally, morphologically normal, motile sperm are selected. Even though there have been debates on usefulness of morphology as a reliable indicator of normal healthy sperm, it is still considered an important factor in ICSI cases [Aston and Weimer 2010]. Density gradient preparation also has been a successful method to isolate normal motile sperm from semen. It consists of filtering sperm by centrifugal force through either one or multiple layers of increasingly concentrated silane-coated silica particles. The process is able to generate a pellet at the bottom of a tube which contains a higher percentage of clean, motile sperm for intrauterine insemination (IUI) [Peterson et al. 2010]. Unlike morphology based methods, PICSI is a biologically inspired technology that mimics the natural attraction between mature sperm and oocytes. A layer of hyaluronan hydrogel at the bottom of a petri dish acts like an oocyte cell, which induces sperm to swim through its surface. Because this technique depends on of sperm, it offers an additional test for normal sperm selection along with morphology based tests [Parmegiani et al. 2012]. Conventional clinical methods mentioned above should be suitable for highly concentrated samples with plenty of motile sperm. However, these methods are not feasible to sperm samples with low concentrations (<100 sperm/ ml) that only contain immotile sperm such as a microtese sample. Use of microfluidics for sperm selection Single-cell analysis has been a driving force of microfluidics since its inception due to an increasing need to understand molecular and cell biology, and to develop better diagnostics and treatments for human disease. Currently, there is a wealth of micro-sized particle/cell separation and sorting techniques that utilize microfluidics and serve a vast array of biomedical applications [Yun et al. 2013; Muetal.2013; Lindström and Andersson-Svahn 2010; Gossettetal. 2010; Bhagatetal.2010; Sajeesh and Sen 2014]. In the field of ART, microfluidic technologies have previously been applied to sperm manipulation for purposes such as analysis, sorting, and separation [Swain et al. 2013]. The most notable methods are summarized in Table 1. In one of the earliest applications, a glass microfluidic chip containing multiple microchannels connecting from an input reservoir to a collecting reservoir, enabled motile sperm to swim to specific reservoirs where they could be collected while removing nonmotile sperm and debris [Tasoglu et al. 2013]. This technology first demonstrated the value of microfluidic platforms for sperm separation [Kricka et al. 1997]. Currently, the most popular microfluidics approach for sperm separation involves flowing parallel laminar streams of media through straight microchannels. One of the first examples of this technique used a polydimethylsiloxane (PDMS) microchannel to introduce a diluted semen sample and media into two separate inlets before they converged into a single microfluidic channel [Cho et al. 2003; Schuster et al. 2003]. At the microscale, the two fluid streams do not mix readily, so only motile sperm are able to travel through the boundary of the two parallel streams. The two streams are separated again after a length sufficient to allow motile sperm to cross the boundary in high numbers. Thus, this strategy allows for separation of motile sperm from non-motile sperm and debris (Figure 2A). Following device optimization, the utility of this technology for ART was verified using sperm collected from the outlet for IVF [Swain et al. 2013; Huang 2014; Huang et al. 2014; Matsuura et al. 2012; Sano et al. 2010; Wu et al. 2006]. Another notable microfluidic approach, which utilizes chemotaxis in addition to for sperm separation, works by inducing sperm to travel through microchannels toward chemo-attractants applied to collection reservoirs at the periphery of the device (Figure 2B) [Koyamaetal.2006; Xieetal.2010; Ko et al. 2012]. A related technique utilizes slow flow and the settling of non-motile sperm at horizontal obstacles within microchannels to separate only motile sperm that can travel over/under the obstacle. The slow flow is passively powered by introducing the sample in an input reservoir, and only motile sperm can travel to the other side of the device while nonmotile sperm and other debris settle at the input reservoir (Figure 2C) [Lopez-Garcia et al. 2008; Ma et al. 2011].

6 SYSTEMS BIOLOGY IN REPRODUCTIVE MEDICINE 165 Table 1. Summary of conventional sperm separation techniques. Mode of Separation/ Method Sorting Microstructures Micro channels + well + sperm Microstructures Linear velocity distribution + sperm Separation/ Sorting Criteria Sperm Sperm Microstructures Sperm chemotaxis + Micro channels Sperm Microstructures Micro obstacle Sperm integrated micro fluidic channel + sperm Microstructures Diffusing + sperm Sperm Optical Lens-less charge Sperm coupled device + sperm Microstructures Electrode integrated micro channels + sperm + electrode Sperm Collected Sample Motile sperm (human/ mouse) Motile sperm (Human, mouse, boar) Application Semen Testing Motile sperm separation Motile sperm Motile sperm (mouse) separation Motile sperm Sperm (bull, mouse) separation/ screening Motile sperm Motile sperm sorting Motile sperm Motile sperm (mouse) sorting/ monitoring Motile sperm Sperm (boar) concentration measurement Collected Sample Condition Purity (%) Efficiency (%) Lost target sample (%) Reference N/A N/A N/A Kricka et al. 1997; Tasoglu et al >90 0.3~60 26~99 Cho et al. 2003; Schuster et al. 2003; Huang 2014; Matsuura et al. 2012; Huang et al. 2014; Wu et al ~100 N/A >99 Koyama et al. 2006; Xie et al. 2010; Ko et al <96.1 N/A N/A Lopez-Garcia et al. 2008; Ma et al N/A N/A N/A Lin et al N/A N/A N/A Zhang et al. 2011a NA N/A N/A Segerink et al Figure 2. Diagrams of conventional sperm separation methods. (A) Sperm separation with parallel larminar flow in straight channel, (B) sperm chemotaxis method (C), micro-obsticle in the channel, and (D) micro-diffuser type channel. In addition to separation technologies, a variety of other microfluidic techniques have been utilized to sort motile sperm, including microdiffusion, lensless charged-couple-devices (CCDs), and electrodeintegrated microchannels. The microdiffuser sorting technique uses a widening channel to spread the flow, which correspondingly lowers the flow speed along the length of the channel (Figure 2D). Motile sperm will swim against the flow and eventually take up a position along the channel where the flow through the channel matches the speed at which the sperm is swimming. Thus, sperm can be separated by, and non-motile sperm will drift to the outlet. [Lin et al. 2013]. The CCD integrated microfluidic channel identifies the shadow of motile sperm through a CCD sensor coupled with image processing software [Zhang et al. 2011a], after which themotilespermcanbedirectedtocollectionreservoirs. The electrode integrated microchannel technology counts individual sperm within flowing media by detecting impedance change of the electrode [Segerink et al. 2010]. In the approaches outlined above, the underlying principle of sperm separation/sorting is, meaning only motile sperm can be separated from the original sample. Thus, while these techniques are of significant clinical value for cases in which motile sperm are present within a semen sample, they are

7 166 R. SAMUEL ET AL. not applicable for microtese tissue specimens since testicular sperm have not yet fully matured or gained. Nonetheless, particle and cell separation techniques that do not rely on have been designed for other applications. Looking ahead: Microfluidics, microtese, and improved sperm selection Microfluidics for clinically feasible sperm manipulation Because recovery of immotile testicular sperm presents a unique set of challenges, current sperm-related microfluidic technologies are not practical for microtese tissue specimens. However, a number of automated microfluidics-based technologies currently exist that could be applied to the microtese procedure without a great deal of difficulty. By using automated technologies, the potential exists to minimize the need for skilled tissue processing personnel, while at the same time increasing the efficiency and consistency of the process in the future, leading to increased sperm recovery rates. In order for a cell/particle separation microfluidic technology to be successful for microtese, it needs to possess the following specific characteristics: (1) Due to their clinical use with ICSI, sperm separations should not involve any labelling of sperm. (2) Because testicular sperm are not fully mature, sperm separation techniques should not rely on. (3) Since the number of sperm present in the sample is typically low, the recovery rate or yield of sperm should be high (~100%). (4) The microfluidic system should be able to account for variation in samples in terms of constituents of the sample. (5) The microfluidic system should work efficiently with small sample volumes (5 10 ml or less). (6) After ensuring that the above requirements are met, the final instrumentation should be manufacturable, sterilizable, simple, and costeffective. Separation techniques reported in the literature that may be most applicable to microtese are listed in Table 2. These techniques may include additional traits, however, only those traits that are needed to meet the above six metrics are included in Table 2. Microfluidics for sperm cryopreservation As mentioned earlier, current clinically adopted technologies for minimum volume vitrification are not suitable to handle small volume samples with very low concentration of cells (e.g., 1 sperm in a volume of 10 µl of buffer solution), which is typical of microtese samples. However, microfluidics is, at its very core, developed for handling very small volumes. Recent reviews and studies have been published that can help the ART community to address problems in effective cryopreservation of sperm from microtese samples by utilizing microfluidic technology [Zhang et al. 2012; Zhang et al. 2011b; Song et al. 2009; Li et al. 2010; Pyne and Liu 2014]. Some of these works that seem promising for single or low number sperm cryopreservation are discussed below. There is significant motivation by the life science community to pursue vitrification of cells in small volumes (less than 1 µl) as it significantly reduces the concentration of cryoprotecting agents (CPA) needed to keep cells viable [Zhang et al. 2011b]. This is achieved by fast cooling rates at microliter or nanoliter sized volumes. Cryoprotecting agents are known to have toxicity effects on cells [Zhang et al. 2011b]. Promising recent results have been shown by immersing nanoliter-sized droplets of mouse oocytes with CPA directly in liquid nitrogen [Zhang et al. 2012]. This process is called droplet-based vitrification [Zhang et al. 2011b]. After retrieval of oocytes from vitrification and 24 hours of culture the authors report comparable survival rates, similar morphology, and similar oocyte parthenogenetic activation to fresh oocytes. Similar success with droplet-based vitrification has been achieved with plant species, and mammalian oocytes and embryos [Zhang et al. 2011b]. Furthermore the effectiveness of droplet-based vitrification relies highly on the size of the droplets; inconsistent size of droplets can have significant effect on the rapid cooling and thawing rates [Song et al. 2010]. The advantage of droplet-based vitrification is that it is based on microfluidic technology and can thus be easily automated, providing consistent droplet size and free of tedious efforts from skilled personnel [Zhang et al. 2012; Zhangetal.2011b]. Potential of microfluidics for selection of viable sperm for IVF In ART a successful outcome depends on the quality of germ cells (oocytes and sperm). Selecting good quality sperm is an essential step in the development of embryos and it is vitally important in cases of male infertility. Sperm are more than a DNA delivery

8 SYSTEMS BIOLOGY IN REPRODUCTIVE MEDICINE 167 Table 2. Types of potential sperm separation techniques for processing samples (microtese with low sperm concentration). Working Method principle Advantages Disadvantages Ref. Comments Microscale Filters Restriction by incorporating microfeatures or fluid physics Simple in concept and design; easy to fabricate/ integrate with other microfluidic systems High likelihood to clogging Gossett et al Works best with low sample volumes, low concentrations, low throughputs 2. May not be ideal for microtese sample due to cell size similarity present in such samples (i.e., red blood cells and sperm heads are of a similar size), the asymmetrical shape of sperm, and the relatively low concentration of sperm compared to other species present in the tissue specimen 3. One type of filter, called crossflow filters may be best for processing microtese Hydrodynamic Filtration and Pinched Flow Fractionation Deterministic lateral displacement (DLD) Inertial microfluidics Dielectrophoresis Utilizes fluid physics at microscale Restriction by incorporating microfeatures or fluid physics Utilizes fluid physics at microscale Relies on the electrophoretic mobility of particles of interest Simple and easy to integrate with other microfluidic components 1. High separation efficiency 2. High separation resolution 3. Easy integration with other microfluidic components and moderate throughput. 1. Moderate separation efficiency 2. Moderate separation resolution 3. Simple design 4. Ease of integration with other microfluidic components 5. High throughput 6. Works best with low sample concentrations 1. High separation efficiency 2. High separation resolution 3. Efficient for small sample volumes Not ideal for separating particles of similar sizes Please refer to associated comment High pressure devices; making devices prone to sample leakages and adding difficulties to fabrication 1. Can be difficult to fabricate and design 2. Certain configurations of a dielectrophoresis setup for cell separation can lead to cell damage Gossett et al. 2010; Sajeesh & Sen 2014 Sajeesh & Sen 2014 Amini et al. 2014; Gossett et al Gossett et al. 2010; Sajeesh & Sen 2014 samples Since these techniques work on similar fluid physics as crossflow filters, they have potential to process microtese samples Separation of a relatively low concentration of non-spherical sperm cells from other cells with small size differences may be difficult using DLD, primarily because the sperm might not present themselves to the array with the same alignment, leading to radically different separation results Recent work from our group shows significant potential for application of inertial microfluidics for processing microtese samples [Son et al. 2015] Microfluidic dielectrophoresis can be considered to be separation technique for microtese samples if polarizability differences can be shown for the cells of interest vehicle; they are now believed to play a crucial role in early and late embryonic development [Barroso et al. 2009]. Thus, development of methods that can identify high quality spermatozoa would definitely improve ART success. Currently, especially in the cases of ICSI, sperm are selected solely based on and morphology parameters, but recent data indicate that normal morphology is not necessarily associated with DNA integrity [Avendaño and Oehninger 2011]. Recent studies have also demonstrated that the role of the male gamete in embryogenesis is significant and can have profound impacts on embryogenesis, pregnancy, and offspring health [Carrell 2013]. Therefore, there is a significant need for more accurate sperm fertilization markers for normal development potential. Development of technology that can accurately select the sperm with the best developmental potential is needed and the technology must be based on knowledge of natural sperm selection mechanisms in vivo and the insights that are gained from the latest research. MicroTESE is one area where microfluidics may be able to have a near-term impact by overcoming challenges with the procedure, such as the time consuming and labor intensive nature of the procedure and the modest pregnancy success rates, and in selecting and finding the best sperm candidates in the sample. Currently the success rate for retrieving sperm via microtese is approximately 54% according to the latest data [Bernie et al. 2015; Ashraf et al. 2014]. There is no available data at the moment demonstrating how often failures are due to technician s error in not finding viable sperm for ICSI. In about 51% of the oocytes, normal fertilization after sperm injection is achieved and a cumulative pregnancy rate is 28% [Ashraf et al. 2014]. The length of time needed for the procedure

9 168 R. SAMUEL ET AL. may be a reason deterring the widespread applicability of microtese and its overall success [Gardner et al. 2011]. In many cases the procedure requires extended laboratory processing to find sperm after failed initial screening. Sample processing can be incredibly labor intensive and the search process may miss the rare spermatozoa within a sea of seminiferous tubules and plethora of other cells [Ramasamy et al. 2011a]. Microfluidics has the potential to improve the speed and efficiency of the process and identify high-quality sperm. In combination with microfluidics, Raman spectroscopy has the potential to help identify the best sperm for ART. Raman spectroscopy is a technique that is used in analytical chemistry to precisely identify the existence and quantity of a particular molecule in a sample. Despite its initial discovery in 1928 [Ramser 2012], Raman spectroscopy has only recently started being used in the analysis of biomolecules, which is mostly due to the recent development and reduction in cost of associated hardware required to capture weak Raman signals. A combination of Raman spectroscopy and microscopy called Raman microspectroscopy is capable of non-invasively identifying molecular characteristics of sperm [Mallidis et al. 2014]. But current Raman microspectroscopy efforts have focused exclusively on dead sperm, fixed to a glass cover slip. Combining Raman microspectroscopy and microfluidics could lead to systems that can trap/sort single live sperm and then measure the quality/quantity of their sub-cellular components [Ramser 2012]. Such systems can be used to select sperm with good molecular characteristics non-invasively before IVF and ICSI procedures, thus increasing fertility outcomes from microtese samples when very few sperm are present. However, progress in this field would require expertise in the fields of Raman spectroscopy, andrology, and microfluidics. This kind of collaboration is very possible in the current age and culture of remarkable interdisciplinary research. For more detailed information on combining Raman spectroscopy and microfluidics, the readers are referred to an in-depth review by Chrimes et al. [2013] and Ramser [2012]. In order for microfluidics to be fully utilized in ART, it will require collaboration between practitioners of reproductive medicine and experts in microfluidics, since microfluidic systems developed to process samples containing rare cells (e.g., microtese), will require creative design and microfabrication skills. Clinical samples are inhomogeneous in constituents; careful and precise design principles must be applied to avoid one of the most simple, but most damaging, issues in microfluidics, clogging of microchannels. Here, the very strength of microfluidics (the microscale fluid domain) can become its downfall. However, with careful thought and preparation in such collaborative efforts (so that the right problem meets the right solution), microfluidics can make its contribution to challenging problems in reproductive medicine. Conclusions It is clear that microfluidic technologies have the potential to be applied to microtese procedures. Many of the particle and cell separation techniques described in this article are suitable for non-motile sperm separation, and devices could be fabricated with little modification from their current state. The combination of two or more of these separation technologies would likely result in efficient sperm recovery from microtese tissue specimens. In addition to replacing the cumbersome manual cell identification step of microtese with automated microfluidic separation of sperm. There are other aspects of microtese that would also benefit from automated or microscale methods, including cryopreservation and the ability to utilize Raman microspectroscopy for identification of genetically fit sperm. Importantly, microfluidic systems are amenable to modulation. Therefore, microscale cryopreservation systems could easily be connected to a sperm separation device for a hands-free, tissue processing technology. Ultimately, a single device that separates sperm (based on genetic fitness) and cryopreserves sperm could simplify the process of microtese. However, these kinds of improvements in microtese procedures can only be achieved by synergistic collaboration between engineers, chemists, and physicians. Declaration of interests Raheel Samuel, Bruce K. Gale, Douglas T. Carrell, and James M. Hotaling have equity in NanoNC Inc. NanoNC is focused on developing innovative solutions for reproductive medicine by utilizing microfluidics technology. Notes on contributors Contributed in sections regarding promising microfluidic technologies for microtese, Raman spectroscopy, small volume cryopreservation, and edited the entire document for submission: RS; Contributed in sections regarding clinical practices of IVF, microtese, cryopreservation, and sperm selection: OB, KEM, DPP, DTC, JMH; Contributed in sections regarding existing microfluidic technology for cell separation: JS; Contributed in sections on microfluidics: BKG.

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