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Vertebrate reproductive science and technology
RESEARCH ARTICLE (Open Access)

Effect of counting chamber depth on the accuracy of lensless microscopy for the assessment of boar sperm motility

Carles Soler A B G , José Á. Picazo-Bueno C , Vicente Micó C , Anthony Valverde A D , Daznia Bompart B , Francisco J. Blasco B , Juan G. Álvarez E F and Almudena García-Molina B
+ Author Affiliations
- Author Affiliations

A University of Valencia, Department of Celular Biology, Functional Biology and Physical Anthropology, Campus Burjassot, C/ Dr Moliner, 50, 46100, Burjassot, Spain.

B Proiser R+D, C/ Catedràtic Agustín Escardino, 9, Building 3 (CUE), Floor 1, 46980, Paterna, Spain.

C University of Valencia, Department of Optics, Campus Burjassot, C/ Dr Moliner, 50, 46100, Burjassot, Spain.

D Technological Institute of Costa Rica, San Carlos Campus, School of Agronomy, 223-21001 Alajuela, Costa Rica.

E Centro ANDROGEN, C/Fernando Macías 8-1°C, 15004, A Coruña, Spain

F Harvard Medical School, Boston, MA, USA.

G Corresponding author. Email: carles.soler@uv.es

Reproduction, Fertility and Development 30(6) 924-934 https://doi.org/10.1071/RD17467
Submitted: 31 October 2017  Accepted: 7 March 2018   Published: 4 May 2018

Journal Compilation © CSIRO 2018 Open Access CC BY-NC-ND

Abstract

Sperm motility is one of the most significant parameters in the prediction of male fertility. Until now, both motility analysis using an optical microscope and computer-aided sperm analysis (CASA-Mot) entailed the use of counting chambers with a depth to 20 µm. Chamber depth significantly affects the intrinsic sperm movement, leading to an artificial motility pattern. For the first time, laser microscopy offers the possibility of avoiding this interference with sperm movement. The aims of the present study were to determine the different motility patterns observed in chambers with depths of 10, 20 and 100 µm using a new holographic approach and to compare the results obtained in the 20-µm chamber with those of the laser and optical CASA-Mot systems. The ISAS®3D-Track results showed that values for curvilinear velocity (VCL), straight line velocity, wobble and beat cross frequency were higher for the 100-µm chambers than for the 10- and 20-µm chambers. Only VCL showed a positive correlation between chambers. In addition, Bayesian analysis confirmed that the kinematic parameters observed with the 100-µm chamber were significantly different to those obtained using chambers with depths of 10 and 20 µm. When an optical analyser CASA-Mot system was used, all kinematic parameters, except VCL, were higher with ISAS®3D-Track, but were not relevant after Bayesian analysis. Finally, almost three different three-dimensional motility patterns were recognised. In conclusion, the use of the ISAS®3D-Track allows for the analysis of the natural three-dimensional pattern of sperm movement.

Additional keywords: CASA-Mot system, kinematic, laser.


References

Allen, M. J., Bradbury, E. M., and Balhorn, R. (1995). The natural subcellular surface structure of the bovine sperm cell. J. Struct. Biol. 114, 197–208.
The natural subcellular surface structure of the bovine sperm cell.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2MzptFCltg%3D%3D&md5=cfbd59f3764a4843563a4724ed3f0b3aCAS |

Amann, R. P., and Waberski, D. (2014). Computer-assisted sperm analysis (CASA): capabilities and potential developments. Theriogenology 81, 5–17.e3.
Computer-assisted sperm analysis (CASA): capabilities and potential developments.Crossref | GoogleScholarGoogle Scholar |

Barratt, C. L. R., Osborn, J. C., Harrison, P. E., Monks, N., Dunphy, B. C., Lenton, E. A., and Cooke, I. D. (1989). The hypo-osmotic swelling test and the sperm mucus penetration test in determining fertilization on the human oocyte. Hum. Reprod. 4, 430–434.
The hypo-osmotic swelling test and the sperm mucus penetration test in determining fertilization on the human oocyte.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1MzgvFWmtA%3D%3D&md5=1cc06c2a582db7270a34e42a759c968fCAS |

Barratt, C. L. R., Björndahl, L., Menkveld, R., and Mortimer, D. (2011). ESHRE Special Interest Group for Andrology basic semen analysis course: a continued focus on accuracy, quality, efficiency and clinical relevance. Hum. Reprod. 26, 3207–3212.
ESHRE Special Interest Group for Andrology basic semen analysis course: a continued focus on accuracy, quality, efficiency and clinical relevance.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MboslyksA%3D%3D&md5=de480160faac30da251c2a96a09f52fdCAS |

Bobe, J., and Labbé, C. (2010). Egg and sperm quality in fish. Gen. Comp. Endocrinol. 165, 535–548.
Egg and sperm quality in fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktVentA%3D%3D&md5=a224f7af520f97b2a3ab3b9af43ce79bCAS |

Böhmer, M., Van, Q., Weyand, I., Hagen, V., Beyermann, M., Matsumoto, M., Hoshi, M., Hilderbrand, E., and Kaupp, U. B. (2005). Ca2+ spikes in the flagellum control chemotactic behaviour of spderm. EMBO J. 24, 2741–2752.
Ca2+ spikes in the flagellum control chemotactic behaviour of spderm.Crossref | GoogleScholarGoogle Scholar |

Bompart, D., García-Molina, A., Valverde, A., Caldeira, C., Yániz, J., Núñez de Murga, M., and Soler, C. (2018). CASA-Mot technology: how results are affected for the frame rate and counting chamber. Reprod. Fertil. Dev. , .
CASA-Mot technology: how results are affected for the frame rate and counting chamber.Crossref | GoogleScholarGoogle Scholar |

Boyers, S. P., Davis, R. O., and Katz, D. F. (1989). Automated semen analysis. Curr. Probl. Obstet. Gynecol. Fertil. 5, 167–200.

Comhaire, F. H. (1993). Methods to evaluate reproductive health of the human male. Reprod. Toxicol. 7, 39–46.
Methods to evaluate reproductive health of the human male.Crossref | GoogleScholarGoogle Scholar |

Coppola, G., Di Caprio, G., Wilding, M., Ferraro, P., Esposito, G., Di Matteo, L., Dale, R., Coppola, G., and Dale, B. (2014). Quantitative label-free animal sperm imaging by means of digital holographic microscopy. IEEE J. Sel. Top. Quantum Electron. 16, 833–840.

Cox, J. F., Zavala, A., Saravia, F., Rivas, C., Gallardo, P., and Alfaro, V. (2002). Differences in sperm migration through cervical mucus in vitro relates to sperm colonization of the oviduct and fertilizing ability in goats. Theriogenology 58, 9–18.
Differences in sperm migration through cervical mucus in vitro relates to sperm colonization of the oviduct and fertilizing ability in goats.Crossref | GoogleScholarGoogle Scholar |

Cui, X., Lee, L. M., Heng, X., Zhong, W., Sternberg, P. W., Psaltis, D., and Yang, C. (2008). Lensless high-resolution on-chip optofluidic microscopes for Caenorhabditis elegans and cell imaging. Proc. Natl Acad. Sci. USA 105, 10670–10675.
Lensless high-resolution on-chip optofluidic microscopes for Caenorhabditis elegans and cell imaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpvFSntLs%3D&md5=44eb2986308eacc905285bfa34104010CAS |

Cummins, J. M. (1982). Hyperactivated motility patterns of ram spermatozoa recovered from the oviducts of mated ewes. Gamete Res. 6, 53–63.
Hyperactivated motility patterns of ram spermatozoa recovered from the oviducts of mated ewes.Crossref | GoogleScholarGoogle Scholar |

Cummins, J. M., and Woodall, P. F. (1985). On mammalian sperm dimensions. J. Reprod. Fertil. 75, 153–175.
On mammalian sperm dimensions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M3pt1yntA%3D%3D&md5=187bf7c37aa4c6fa3b6a3182c67f879dCAS |

de Wagenaar, B., Dekker, S., de Boer, H. L., Bomer, J. G., Olthuis, W., van der Berg, A., and Segerink, Ll. (2016). Towards microfluidic sperm refinement: impedance-base analysis and sorting of sperm cells. Lab Chip 16, 1514–1522.
Towards microfluidic sperm refinement: impedance-base analysis and sorting of sperm cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XktFChsLw%3D&md5=9fe5c31ff67e57df7655bcdc679c8c0eCAS |

Di Caprio, G., Ferrara, M. A., Miccio, L., Merola, F., Memmolo, P., Ferraro, P., and Coppola, G. (2015). Holographic imaging of unlabelled sperm cells for semen analysis: a review. J. Biophotonics 8, 779–789.
Holographic imaging of unlabelled sperm cells for semen analysis: a review.Crossref | GoogleScholarGoogle Scholar |

Di Rienzo, J. A., Casanoves, F., Balzarini, M. G., Gonzalez, L., Tablada, M., and Robledo, C. W. (2017). InfoStat versión 2017. (Grupo InfoStat, FCA, Universidad Nacional de Córdoba: Córdoba, Argentina.) Available at http://www.infostat.com.ar [verified 12 April 2018].

Elgeti, J., Kaupp, U. B., and Gompper, G. (2010). Hydrodynamics of sperm cells near surfaces. Biophys. J. 99, 1018–1026.
Hydrodynamics of sperm cells near surfaces.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaqt7nK&md5=7e492012fc4c40029431038a20c59f28CAS |

ESHRE Andrology Special Interest Group (1996). Consensus workshop on advanced diagnostic andrology techniques. Hum. Reprod. 11, 1463–1479.
Consensus workshop on advanced diagnostic andrology techniques.Crossref | GoogleScholarGoogle Scholar |

Fraser, L. R. (1977). Motility patterns in mouse spermatozoa before and after capacitation. J. Exp. Zool. 202, 439–444.
Motility patterns in mouse spermatozoa before and after capacitation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1c%2FmvVSmtA%3D%3D&md5=6bddc250462452428ebb44599aca2f87CAS |

Frentz, Z., Kuehn, S., Hekstra, D., and Leibler, S. (2010). Microbial population dynamics by digital in-line holographic microscopy. Rev. Sci. Instrum. 81, 084301.
Microbial population dynamics by digital in-line holographic microscopy.Crossref | GoogleScholarGoogle Scholar |

Fürhapter, S., Jesacher, A., Bernet, S., and Ritsch-Marte, M. (2005). Spiral phase contrast imaging in microscopy. Opt. Express 13, 689–694.
Spiral phase contrast imaging in microscopy.Crossref | GoogleScholarGoogle Scholar |

Gabor, D. (1948). A new microscopic principle. Nature 161, 777–778.
A new microscopic principle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaH1c%2FgsVSgug%3D%3D&md5=bae55289dbcac6cc5811a03951777df2CAS |

Geyer, C. (1992). Practical Markov chain Monte Carlo. Stat. Sci. 7, 473–483.
Practical Markov chain Monte Carlo.Crossref | GoogleScholarGoogle Scholar |

Greenbaum, A., Luo, W., Su, T. W., Göröcs, Z., Xue, L., Isikman, S. O., Coskun, A. F., Mudanyali, O., and Ozcan, A. (2012). Imaging without lenses: achievements and remaining challenges of wide-field on-chip microscopy. Nat. Methods 9, 889–895.
Imaging without lenses: achievements and remaining challenges of wide-field on-chip microscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1ynt7rL&md5=2c22b56bd09841cfaa99e9e814f0073bCAS |

Greenbaum, A., Akbari, N., Feizi, A., Luo, W., and Ozcan, A. (2013). Field-portable pixel super-resolution colour microscope. PLoS One 8, e76475.
Field-portable pixel super-resolution colour microscope.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFOntb7F&md5=b634c6b14e0b11ad5f7d20f89dad8f3aCAS |

Guzick, D. S., Overstreet, J. W., Factor-Litvak, P., Brazil, C. K., Nakajima, S. T., Coutifaris, C., Carson, S. A., Cisneros, P., Steinkampf, M. P., Hill, J. A., Xu, D., Phil, M., and Vogel, D. L. (2001). Sperm morphology, motility and concentration in fertile and infertile men. N. Engl. J. Med. 345, 1388–1393.
Sperm morphology, motility and concentration in fertile and infertile men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2FmsFGjug%3D%3D&md5=494ae7ffbad21a7403cd6f79d8fc9a43CAS |

Hay, M. A., King, W. A., Gartley, C. J., Leibo, S. P., and Goodrowe, K. L. (1997). Canine spermatozoa – cryopreservation and evaluation of gamete interaction. Theriogenology 48, 1329–1342.
Canine spermatozoa – cryopreservation and evaluation of gamete interaction.Crossref | GoogleScholarGoogle Scholar |

Heng, X., Erickson, D., Baugh, L. R., Yaqoob, Z., Sternberg, P. W., Psaltis, D., and Yang, C. (2006). Optofluidic microscopy – a method for implementing a high resolution optical microscope on a chip. Lab Chip 6, 1274–1276.
Optofluidic microscopy – a method for implementing a high resolution optical microscope on a chip.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFymsr3K&md5=37684c13dc8cb9100ad68a4ebc0c5660CAS |

Hoffman, R., and Gross, L. (1975). Modulation contrast microscope. Appl. Opt. 14, 1169–1176.
Modulation contrast microscope.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c7gsl2qtw%3D%3D&md5=d23a8f47906b8942ad6512666766c8b7CAS |

Holt, W. V., and Van Look, K. J. W. (2004). Concepts in sperm heterogeneity, sperm selection and sperm competition as biological foundations for laboratory tests of semen quality. Reproduction 127, 527–535.
Concepts in sperm heterogeneity, sperm selection and sperm competition as biological foundations for laboratory tests of semen quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkvFOqurk%3D&md5=9c352ede76f040570f97f3b5d2adc3dcCAS |

Hunter, R. H., Coy, P., Gadea, J., and Rath, D. (2011). Considerations of viscosity in the preliminaries to mammalian fertilization. J. Assist. Reprod. Genet. 28, 191–197.
Considerations of viscosity in the preliminaries to mammalian fertilization.Crossref | GoogleScholarGoogle Scholar |

Iglesias, I. (2011). Pyramid phase microscopy. Opt. Lett. 36, 3636–3638.
Pyramid phase microscopy.Crossref | GoogleScholarGoogle Scholar |

Isikman, S. O., Bishara, W., Sikora, U., Yaglidere, O., Yeah, J., and Ozcan, A. (2011). Field-portable lensfree tomographic microscope. Lab Chip 11, 2222–2230.
Field-portable lensfree tomographic microscope.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsV2itrY%3D&md5=ac2d9b302a97905f7edab5029d4fe2b7CAS |

Jericho, S. K., Garcia-Sucerquia, J., Xu, W., Jericho, M. H., and Kreuzer, H. J. (2006). Submersible digital in-line holographic microscope. Rev. Sci. Instrum. 77, 043706.
Submersible digital in-line holographic microscope.Crossref | GoogleScholarGoogle Scholar |

Katz, D. F., Mills, R. N., and Pritchett, T. R. (1978). The movement of human spermatozoa in cervical mucus. J. Reprod. Fertil. 53, 259–265.
The movement of human spermatozoa in cervical mucus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1M%2Fgslegsg%3D%3D&md5=ba7a52e0aa729613613bbbca99a9b628CAS |

Kim, M. K. (2010). Principles and techniques of digital holographic microscopy. SPIE Rev 1, 018005.
Principles and techniques of digital holographic microscopy.Crossref | GoogleScholarGoogle Scholar |

Knowlton, S. M., Sadasivam, M., and Tasoglu, S. (2015). Microfluidics for sperm research. Trends Biotechnol. 33, 221–229.
Microfluidics for sperm research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkvF2rt7g%3D&md5=b783f819811da3f4bb16472bc94a1413CAS |

Lee, M., Yaglidere, O., and Ozcan, A. (2011). Field-portable reflection and transmission microscopy based on lensless holography. Biomed. Opt. Express 2, 2721–2730.
Field-portable reflection and transmission microscopy based on lensless holography.Crossref | GoogleScholarGoogle Scholar |

Lee, S. A., Erath, J., Zheng, G., Ou, X., Willems, P., Eichinger, D., Rodriguez, A., and Yang, C. (2014). Imaging and identification of waterborne parasites using a chip-scale microscope. PLoS One 9, e89712.
Imaging and identification of waterborne parasites using a chip-scale microscope.Crossref | GoogleScholarGoogle Scholar |

Lenz, R. W., Kjelland, M. E., VonderHaar, K., Swannack, T. M., and Moreno, J. F. (2011). A comparison of bovine seminal quality assessments using different viewing chambers with a computer-assisted semen analyser. J. Anim.Sci. 89, 383–388.
A comparison of bovine seminal quality assessments using different viewing chambers with a computer-assisted semen analyser.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvFSnur4%3D&md5=d8394f3ee5261113d086b9ddb0951ee3CAS |

Lu, J. C., Huang, Y. F., and Lü, N. Q. (2014). Computer-aided sperm analysis: past, present and future. Andrologia 46, 329–338.
Computer-aided sperm analysis: past, present and future.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3srhslKjsw%3D%3D&md5=ff0224ea4a67ff8f3b41f14b44fbaa1dCAS |

Majeed, H., Sridharan, S., Mir, M., Ma, L., and Popescu, G. (2017). Quantitative phase imaging for medical diagnosis J. Biophotonics 10, 177–205.
Quantitative phase imaging for medical diagnosisCrossref | GoogleScholarGoogle Scholar |

Marquet, P., Depeursinge, C., and Magistretti, P. J. (2014). Review of quantitative phase-digital holographic microscopy: promising novel imaging technique to resolve neuronal network activity and identify cellular biomarkers of psychiatric disorders. Neurophotonics 1, 020901.
Review of quantitative phase-digital holographic microscopy: promising novel imaging technique to resolve neuronal network activity and identify cellular biomarkers of psychiatric disorders.Crossref | GoogleScholarGoogle Scholar |

McLeskey, S. B., Dowds, C., Carballada, R., White, R. R., and Sailing, P. M. (1997). Molecules involved in mammalian sperm–egg interaction. Int. Rev. Cytol. 177, 57–113.
Molecules involved in mammalian sperm–egg interaction.Crossref | GoogleScholarGoogle Scholar |

Memmolo, P., Di Caprio, G., Distante, C., Paturzo, M., Puglisi, R., Balduzzi, D., Galli, A., Coppola, G., and Ferraro, P. (2011). Identification of bovine sperm head for morphometry analysis in quantitative phase-contrast holographic microscopy. Opt. Express 19, 23215–23226.
Identification of bovine sperm head for morphometry analysis in quantitative phase-contrast holographic microscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFKqtbjJ&md5=99173f308c130307400b7dd1f8d4d3afCAS |

Memmolo, P., Miccio, L., Paturzo, M., Di Caprio, G., Coppola, G., Netti, P. A., and Ferraro, P. (2015). Recent advances in holographic 3D particle tracking. Adv. Opt. Photonics 7, 713–755.
Recent advances in holographic 3D particle tracking.Crossref | GoogleScholarGoogle Scholar |

Mengerink, K. J., and Vacquier, V. D. (2001). Glycobiology of sperm–egg interactions in deuterostomes. Glycobiology 11, 37R–43R.
Glycobiology of sperm–egg interactions in deuterostomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvFGlu7Y%3D&md5=c53fc25d2bf1364a2b21417240f0919dCAS |

Merola, F., Miccio, L., Memmoloa, P., Di Caprio, G., Galli, A., Puglisi, R., Balduzzi, D., Coppola, G., Netti, P., and Ferraro, P. (2013). Digital holography as a method for 3D imaging and estimating the biovolume of motile cells. Lab Chip 13, 4512–4516.
Digital holography as a method for 3D imaging and estimating the biovolume of motile cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVWgs7vO&md5=47903709da5a63240905fcbb24f006a3CAS |

Micó, V., Ferreira, C., Zalevsky, Z., and García, J. (2010). Basic principles and applications of digital holographic microscopy. In ‘Microscopy: Science Technology, Applications and Education’. (Eds A. Méndez-Vilas and J. Díaz.) pp. 1411–1418. (Formatex Research Center: Badajoz, Spain.)

Morales, P., Overstreet, J. W., and Katz, D. F. (1988). Changes in human sperm motion during capacitation in vitro. J. Reprod. Fertil. 83, 119–128.
Changes in human sperm motion during capacitation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c3os1Gjug%3D%3D&md5=dc69c91a2e0751fb32b600097b368545CAS |

Mortimer, S. T., and Swan, M. A. (1995a). Variable kinematics of capacitating human spermatozoa. Hum. Reprod. 10, 3178–3182.
Variable kinematics of capacitating human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28vhvFKrsg%3D%3D&md5=5e1e6a72bd20524fc7ad2a494df814feCAS |

Mortimer, S. T., and Swan, M. A. (1995b). Kinematics of capacitating human spermatozoa analysed at 60 Hz. Hum. Reprod. 10, 873–879.
Kinematics of capacitating human spermatozoa analysed at 60 Hz.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2MznvVeqtQ%3D%3D&md5=06d6a2f9502a67d3c8caea85d36b8321CAS |

Mortimer, S. T., Schoëvaërt, D., Swan, M. A., and Mortimer, D. (1997). Quantitative observations of flagellar motility of capacitating human spermatozoa. Hum. Reprod. 12, 1006–1012.
Quantitative observations of flagellar motility of capacitating human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szjsl2rtg%3D%3D&md5=470fc88b74b2c9ccc6bd8a5ed3326551CAS |

Morton, D. B., and Glover, T. D. (1974). Sperm transport in female rabbit: the rôle of the cervix J. Reprod. Fertil. 38, 131–138.
| 1:STN:280:DyaE2c3nsFWkuw%3D%3D&md5=d55c5c4ae520a438944942d8670e6bfeCAS |

Mudanyali, O., Oztoprak, C., Tseng, D., Erlinger, A., and Ozcan, A. (2010a). Detection of waterborne parasites using field-portable and cost-effective lensfree microscopy. Lab Chip 10, 2419–2423.
Detection of waterborne parasites using field-portable and cost-effective lensfree microscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVKrs7jL&md5=2aad355aa7d20c644f9fc9e94cc59667CAS |

Mudanyali, O., Tseng, D., Oh, C., Isikman, S. O., Sencan, I., Bishara, W., Oztoprak, C., Seo, S., Khademhosseini, B., and Ozcan, A. (2010b). Compact, light-weight and cost-effective microscope based on lensless incoherent holography for telemedicine applications. Lab Chip 10, 1417–1428.
Compact, light-weight and cost-effective microscope based on lensless incoherent holography for telemedicine applications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFOit74%3D&md5=c270fe6622e4c2926848c75ca2b9c0d7CAS |

Nixon, B., Aitken, R. J., and McLaughlin, E. A. (2007). New insights into molecular mechanisms of sperm–egg interaction. Cell. Mol. Life Sci. 64, 1805–1823.
New insights into molecular mechanisms of sperm–egg interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXovFagtLo%3D&md5=da929d08dadd05fe8f4df85a5667e4e6CAS |

Ola, B., Afnan, N., Papioannou, S., Sharif, K., Bjorndahl, L., and Coomarasamy, A. (2003). Accuracy of sperm–cervical mucus penetration tests in evaluation sperm motility in semen: a systematic quantitative review. Hum. Reprod. 18, 1037–1046.
Accuracy of sperm–cervical mucus penetration tests in evaluation sperm motility in semen: a systematic quantitative review.Crossref | GoogleScholarGoogle Scholar |

Olson, S. D., Suarez, S. S., and Fauci, L. J. (2011). Coupling biochemistry and hydrodynamics captures hyperactivated sperm motility in a simple flagellar model. J. Theor. Biol. 283, 203–216.
Coupling biochemistry and hydrodynamics captures hyperactivated sperm motility in a simple flagellar model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpt1ygsb4%3D&md5=5c241eb28a48c212ed5c1d61ff55bda2CAS |

Perucho, B., and Micó, V. (2014). Wavefront holoscopy: application of digital in-line holography for the inspection of engraved marks in progressive addition lenses. J. Biomed. Opt. 19, 16017.
Wavefront holoscopy: application of digital in-line holography for the inspection of engraved marks in progressive addition lenses.Crossref | GoogleScholarGoogle Scholar |

Popescu, G. (2011). ‘Quantitative Phase Imaging of Cells and Tissues.’ (McGraw-Hill Professional: New York.)

Pushkarsky, I., Liu, Y., Weaver, W., Su, T. W., Mudanyali, O., Ozcan, A., and Di Carlo, D. (2014). Automated single-cell motility analysis on a chip using lensfree microscopy. Sci. Rep. 4, 4717.

Repetto, L., Piano, E., and Pontiggia, C. (2004). Lensless digital holographic microscope with light-emitting diode illumination. Opt. Lett. 29, 1132–1134.
Lensless digital holographic microscope with light-emitting diode illumination.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c3otF2rsQ%3D%3D&md5=68b8d2784ba9eb66e0a1c0a86506bfbcCAS |

Rikmenspoel, R. (1984). Movements of bull sperm flagella as a function of temperature and viscosity. J. Exp. Biol. 108, 205–230.
| 1:STN:280:DyaL2c7mtlOnuw%3D%3D&md5=956e399a16940d119e8ae960f80cf3c1CAS |

Rogers, G. L. (1952). XIV. – Experiments in diffraction microscopy. Proc. Roy. Soc. Edinburgh Sect. A 63, 193–221.
XIV. – Experiments in diffraction microscopy.Crossref | GoogleScholarGoogle Scholar |

Sanz, M., Picazo-Bueno, J. A., García, J., and Micó, V. (2015). Improved quantitative phase imaging in lensless microscopy by single-shot multi-wavelength illumination using a fast convergence algorithm. Opt. Express 23, 21352–21365.
Improved quantitative phase imaging in lensless microscopy by single-shot multi-wavelength illumination using a fast convergence algorithm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXjsFOnsLo%3D&md5=6e87f40ed08e1d48aee3e501751a0aeeCAS |

Sanz, M., Picazo-Bueno, J. A., Granero, L., García, J., and Mico, V. (2017). Compact, cost-effective and field-portable microscope prototype based on MISHELF microscopy. Sci. Rep. 7, 43291.
Compact, cost-effective and field-portable microscope prototype based on MISHELF microscopy.Crossref | GoogleScholarGoogle Scholar |

Satake, N., Elliott, R. M., Watson, P. F., and Holt, W. V. (2006). Sperm selection and activation in pigs may be mediated by the differential motility activation and suppression of sperm populations within the oviduct. J. Exp. Biol. 209, 1560–1572.
Sperm selection and activation in pigs may be mediated by the differential motility activation and suppression of sperm populations within the oviduct.Crossref | GoogleScholarGoogle Scholar |

Shaked, N., Zalevsky, Z., and Satterwhite, L. L. (2012). ‘Biomedical Optical Phase Microscopy and Nanoscopy.’ (Elsevier: Amsterdam.)

Situ, G., Warber, M., Pedrini, G., and Osten, W. (2010). Phase contrast enhancement in microscopy using spiral phase filtering. Opt. Commun. 283, 1273–1277.
Phase contrast enhancement in microscopy using spiral phase filtering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1Wmt74%3D&md5=118dcec24e2bd0ea31871deb37240b30CAS |

Smith, D. J., Gaffney, E. A., Gadêlha, H., Kapur, N., and Kirkman-Brown, J. C. (2009). Bend propagation in the flagella of migrating human sperm, and its modulation by viscosity. Cell Motil. Cytoskeleton 66, 220–236.
Bend propagation in the flagella of migrating human sperm, and its modulation by viscosity.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3itlKrsQ%3D%3D&md5=3ab2e00b5ffcbe710a6fa842f0296e87CAS |

Sobrero, A. J., and MacLeod, J. (1962). The immediate postcoital test. Fertil. Steril. 13, 184–189.
The immediate postcoital test.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF387gs1ejug%3D%3D&md5=3bbfe69407d2003a4fffd17f542c4b45CAS |

Soler, C., Cooper, T. G., Valverde, A., and Yániz, J. (2016). Afterword to Sperm morphometrics today and tomorrow special issue in Asian Journal of Andrology. Asian J. Androl. 18, 895–897.
Afterword to Sperm morphometrics today and tomorrow special issue in Asian Journal of Andrology.Crossref | GoogleScholarGoogle Scholar |

Sorensen, D., and Gianola, D. (2002). ‘Likelihood, Bayesian, and MCMC Methods in Quantitative Genetics.’ 1st edn. (Springer-Verlag: New York.)

Spehr, M., Gisselmann, G., Poplawski, A., Riffell, J. A., Wetzel, C. H., Zimmer, P. K., and Hatt, H. (2003). Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299, 2054–2058.
Identification of a testicular odorant receptor mediating human sperm chemotaxis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitlCis7k%3D&md5=d885062f49f8dddc1e12e4e2971b25a8CAS |

Su, T.-W., Xue, L., and Ozcan, A. (2012). High-throughput lensfree 3D tracking of human sperms reveals rare statistics of helical trajectories. Proc. Natl Acad. Sci. USA 109, 16018–16022.
High-throughput lensfree 3D tracking of human sperms reveals rare statistics of helical trajectories.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFGhs7fP&md5=2ef7525704664884a20af5ae4e00241bCAS |

Su, T.-W., Choi, I., Feng, J., Huang, K., McLeod, E., and Ozcan, A. (2013). Sperm trajectories form chiral ribbons. Sci. Rep. 3, 1664.
Sperm trajectories form chiral ribbons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVansrrI&md5=bf6632a7014079d70cb35a3db99913acCAS |

Teves, M. E., Barbano, F., Guidobaldi, H. A., Sanchez, R., Miska, W., and Giojalas, L. C. (2006). Progesterone at the picomolar range is a chemoattractant for mammalian spermatozoa. Fertil. Steril. 86, 745–749.
Progesterone at the picomolar range is a chemoattractant for mammalian spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFCqsLzJ&md5=f174dccfdf5acc5fcc8a232fc9d8806bCAS |

Tredway, D. R., Fordney-Settlage, D., Nakamura, R. M., Motoshima, M., Umezaki, C. U., and Mishell, R. D. (1975). Significance of timing for the postcoital evaluation of cervical mucus. Am. J. Obstet. Gynecol. 121, 387–393.
Significance of timing for the postcoital evaluation of cervical mucus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2M7gs1OhtA%3D%3D&md5=67673d80b4cc04b741f015c6cd60d4feCAS |

van Gestel, R. A., Brewis, I. A., Ashton, P. R., Brouwers, J. F., and Gadella, B. M. (2007). Multiple proteins present in the purified porcine sperm apical plasma membranes interact with the zona pellucida of the oocyte. Mol. Hum. Reprod. 13, 445–454.
Multiple proteins present in the purified porcine sperm apical plasma membranes interact with the zona pellucida of the oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotl2qurg%3D&md5=d4208d1ce12344e6514af6a82df28fd2CAS |

Woolley, D. M. (2003). Motility of sperm at surfaces. Reproduction 126, 259–270.
Motility of sperm at surfaces.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntFyjtrg%3D&md5=a0252d4714c750d11cee38dae38ea5dbCAS |

World Health Organization (WHO) (1992). ‘WHO Laboratory Manual for the Examination of Human Semen and Sperm–Cervical Mucus Interaction.’ 3rd edn. (Cambridge University Press: New York.)

World Health Organization (WHO) (2010). ‘WHO Laboratory Manual for the Examination and Processing of Human Semen.’ 5th edn. (WHO: Switzerland)

Yanagimachi, R. (1970). The movement of golden hamster spermatozoa before and after capactiation. J. Reprod. Fertil. 23, 193–196.
The movement of golden hamster spermatozoa before and after capactiation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE3M%2FhtFCrtQ%3D%3D&md5=1714a51b3f48b820dd02c6593ab15f23CAS |

Yániz, J. L., Soler, C., and Santolaria, P. (2015). Computer assisted sperm morphometry in mammals: a review. Anim. Reprod. Sci. 156, 1–12.
Computer assisted sperm morphometry in mammals: a review.Crossref | GoogleScholarGoogle Scholar |

Zernike, F. (1942a). Phase contrast, a new method for the microscopic observation of transparent objects Part I. Physica 9, 686–698.

Zernike, F. (1942b). Phase contrast, a new method for the microscopic observation of transparent objects Part II. Physica 9, 974–986.