CASA: tracking the past and plotting the future
M. T. Gallagher A B C , D. J. Smith A B C and J. C. Kirkman-Brown B C D
+ Author Affiliations
- Author Affiliations
A School of Mathematics, University of Birmingham, Birmingham, B15 2TT, UK.
B Institute for Metabolism and Systems Research, University of Birmingham, Birmingham, B15 2TT, UK.
C Centre for Human Reproductive Science, Birmingham Women’s and Children’s NHS Foundation Trust, Birmingham, B15 2TG, UK.
D Corresponding author. Email: j.kirkmanbrown@bham.ac.uk
Reproduction, Fertility and Development 30(6) 867-874 https://doi.org/10.1071/RD17420
Submitted: 12 October 2017 Accepted: 6 April 2018 Published: 29 May 2018
Journal Compilation © CSIRO 2018 CC BY
Abstract
The human semen sample carries a wealth of information of varying degrees of accessibility ranging from the traditional visual measures of count and motility to those that need a more computational approach, such as tracking the flagellar waveform. Although computer-aided sperm analysis (CASA) options are becoming more widespread, the gold standard for clinical semen analysis requires trained laboratory staff. In this review we characterise the key attitudes towards the use of CASA and set out areas in which CASA should, and should not, be used and improved. We provide an overview of the current CASA landscape, discussing clinical uses as well as potential areas for the clinical translation of existing research technologies. Finally, we discuss where we see potential for the future of CASA, and how the integration of mathematical modelling and new technologies, such as automated flagellar tracking, may open new doors in clinical semen analysis.
Additional keywords: clinical diagnostics, flagellar analysis, glyphs, image analysis, machine learning, mathematical modelling, sperm, viscosity.
References
Björndahl, L., Kirkman-Brown, J., Hart, G., Rattle, S., and Barratt, C. L. R. (2006). Development of a novel home sperm test. Hum. Reprod. 21, 145–149.| Development of a novel home sperm test.Crossref | GoogleScholarGoogle Scholar |
Brokaw, C. J. (1966). Effects of increased viscosity on the movements of some invertebrate spermatozoa. J. Exp. Biol. 45, 113–139.
Brokaw, C. J. (1971). Bend propagation by a sliding filament model for flagella. J. Exp. Biol. 55, 289–304.
Brokaw, C. J. (1975). Effects of viscosity and ATP concentration on the movement of reactivated sea-urchin sperm flagella. J. Exp. Biol. 62, 701–719.
Brokaw, C. J. (1991). Calcium sensors in sea urchin sperm flagella. Cell Motil. Cytoskeleton 18, 123–130.
| Calcium sensors in sea urchin sperm flagella.Crossref | GoogleScholarGoogle Scholar |
Casslén, B. (1986). Uterine fluid volume. Cyclic variations and possible extrauterine contributions. J. Reprod. Med. 31, 506–510.
Corkidi, G., Taboada, B., Wood, C. D., Guerrero, A., and Darszon, A. (2008). Tracking sperm in three-dimensions. Biochem. Biophys. Res. Commun. 373, 125–129.
| Tracking sperm in three-dimensions.Crossref | GoogleScholarGoogle Scholar |
Cortez, R., Fauci, L., and Medovikov, A. (2005). The method of regularized Stokeslets in three dimensions: analysis, validation, and application to helical swimming. Phys. Fluids 17, 031504.
| The method of regularized Stokeslets in three dimensions: analysis, validation, and application to helical swimming.Crossref | GoogleScholarGoogle Scholar |
Cosson, J., Huitorel, P., and Gagnon, C. (2003). How spermatozoa come to be confined to surfaces. Cell Motil. Cytoskeleton 54, 56–63.
| How spermatozoa come to be confined to surfaces.Crossref | GoogleScholarGoogle Scholar |
Crenshaw, H. C. (1990). Helical orientation – a novel mechanism for the orientation of microorganisms. In ‘Biological Motion’. (Eds W. Alt and G. Hoffmann.) pp. 361–386. (Springer: Berlin, Heidelberg.)
Crha, I., Zakova, J., Huser, M., Ventruba, P., Lousova, E., and Pohanka, M. (2011). Digital holographic microscopy in human sperm imaging. J. Assist. Reprod. Genet. 28, 725–729.
| Digital holographic microscopy in human sperm imaging.Crossref | GoogleScholarGoogle Scholar |
da Silva, P. A. P. (2017). Quantitative image analysis of cells using morphodynamical models: sea urchin spermatozoa as case study. Ph.D. Thesis, Intituto de Technologia Quimica E Biologica Antonion Xavier (I.T.Q.B.) Universidade Nova de Lisboa.
Daloglu, M. U., and Ozcan, A. (2017). Computational imaging of sperm locomotion. Biol. Reprod. 97, 182–188.
| Computational imaging of sperm locomotion.Crossref | GoogleScholarGoogle Scholar |
Denissenko, P., Kantsler, V., Smith, D. J., and Kirkman-Brown, J. (2012). Human spermatozoa migration in microchannels reveals boundary-following navigation. Proc. Natl Acad. Sci. USA 109, 8007–8010.
| Human spermatozoa migration in microchannels reveals boundary-following navigation.Crossref | GoogleScholarGoogle Scholar |
Di Caprio, G., Gioffre, M. A., Saffioti, N., Grilli, S., Ferraro, P., Puglisi, R., Balduzzi, D., Galli, A., and Coppola, G. (2010). Quantitative label-free animal sperm imaging by means of digital holographic microscopy. IEEE J. Sel. Top. Quant. 16, 833–840.
| Quantitative label-free animal sperm imaging by means of digital holographic microscopy.Crossref | GoogleScholarGoogle Scholar |
Di Caprio, G., El Mallahi, A., Ferraro, P., Dale, R., Coppola, G., Dale, B., Coppola, G., and Dubois, F. (2014). 4D tracking of clinical seminal samples for quantitative characterization of motility parameters. Biomed. Opt. Express 5, 690–700.
| 4D tracking of clinical seminal samples for quantitative characterization of motility parameters.Crossref | GoogleScholarGoogle Scholar |
Douglas-Hamilton, D. H., Smith, N. G., Kuster, C. E., Vermeiden, J. P. W., and Althouse, G. C. (2005). Capillary-loaded particle fluid dynamics: effect on estimation of sperm concentration. J. Androl. 26, 115–122.
Duffy, B., Thiyagalingam, J., Walton, S., Smith, D. J., Trefethen, A., Kirkman-Brown, J. C., Gaffney, E. A., and Chen, M. (2015). Glyph-based video visualization for semen analysis. IEEE Trans. Vis. Comput. Graph. 21, 980–993.
| Glyph-based video visualization for semen analysis.Crossref | GoogleScholarGoogle Scholar |
Flint, M., Plessis, S. S., and Menkveld, R. (2014). Revisiting the assessment of semen viscosity and its relationship to leucocytospermia. Andrologia 46, 837–841.
| Revisiting the assessment of semen viscosity and its relationship to leucocytospermia.Crossref | GoogleScholarGoogle Scholar |
Ford, W. C. L. (2006). Glycolysis and sperm motility: does a spoonful of sugar help the flagellum go round? Hum. Reprod. Update 12, 269–274.
| Glycolysis and sperm motility: does a spoonful of sugar help the flagellum go round?Crossref | GoogleScholarGoogle Scholar |
Friedrich, B. M., and Jülicher, F. (2009). Steering chiral swimmers along noisy helical paths. Phys. Rev. Lett. 103, 068102.
| Steering chiral swimmers along noisy helical paths.Crossref | GoogleScholarGoogle Scholar |
Gabor, D. (1948). A new microscopic principle. Nature 161, 777–778.
| A new microscopic principle.Crossref | GoogleScholarGoogle Scholar |
Gaffney, E. A., Gadêlha, H., Smith, D. J., Blake, J. R., and Kirkman-Brown, J. C. (2011). Mammalian sperm motility: observation and theory. Annu. Rev. Fluid Mech. 43, 501–528.
| Mammalian sperm motility: observation and theory.Crossref | GoogleScholarGoogle Scholar |
Gallagher, M. T., Neal, C. V., Arkill, K. P., and Smith, D. J. (2017). Model-based image analysis of a tethered Brownian fibre for shear stress sensing. J. R. Soc. Interface 14, 20170564.
| Model-based image analysis of a tethered Brownian fibre for shear stress sensing.Crossref | GoogleScholarGoogle Scholar |
Garcia-Sucerquia, J., Xu, W., Jericho, S. K., Klages, P., Jericho, M. H., and Kreuzer, H. J. (2006). Digital in-line holographic microscopy. Appl. Opt. 45, 836–850.
| Digital in-line holographic microscopy.Crossref | GoogleScholarGoogle Scholar |
Gillies, E. A., Cannon, R. M., Green, R. B., and Pacey, A. A. (2009). Hydrodynamic propulsion of human sperm. J. Fluid Mech. 625, 445–474.
| Hydrodynamic propulsion of human sperm.Crossref | GoogleScholarGoogle Scholar |
Goodman, J. W., and Lawrence, R. W. (1967). Digital image formation from electronically detected holograms. Appl. Phys. Lett. 11, 77–79.
| Digital image formation from electronically detected holograms.Crossref | GoogleScholarGoogle Scholar |
Gray, J., and Hancock, G. J. (1955). The propulsion of sea-urchin spermatozoa. J. Exp. Biol. 32, 802–814.
Guerrero, A., Carneiro, J., Pimentel, A., Wood, C. D., Corkidi, G., and Darszon, A. (2011). Strategies for locating the female gamete: the importance of measuring sperm trajectories in three spatial dimensions. Mol. Hum. Reprod. 17, 511–523.
| Strategies for locating the female gamete: the importance of measuring sperm trajectories in three spatial dimensions.Crossref | GoogleScholarGoogle Scholar |
Hiramoto, Y., and Baba, S. A. (1978). A quantitative analysis of flagellar movement in echinoderm spermatozoa. J. Exp. Biol. 76, 85–104.
Holt, W. V., Moore, H. D. M., and Hillier, S. G. (1985). Computer-assisted measurement of sperm swimming speed in human semen: correlation of results with in vitro fertilization assays. Fertil. Steril. 44, 112–119.
| Computer-assisted measurement of sperm swimming speed in human semen: correlation of results with in vitro fertilization assays.Crossref | GoogleScholarGoogle Scholar |
Hyun, N., Chandsawangbhuwana, C., Yang-Wong, C., Berns, M. W., Zhu, Q., and Shi, L. Z. (2012). Effects of viscosity on sperm motility studied with optical tweezers. J. Biomed. Opt. 17, 025005.
| Effects of viscosity on sperm motility studied with optical tweezers.Crossref | GoogleScholarGoogle Scholar |
Ishimoto, K., Gadêlha, H., Gaffney, E. A., Smith, D. J., and Kirkman-Brown, J. (2017). Coarse-graining the fluid flow around a human sperm. Phys. Rev. Lett. 118, 124501.
| Coarse-graining the fluid flow around a human sperm.Crossref | GoogleScholarGoogle Scholar |
Ivic, A., Onyeaka, H., Girling, A., Brewis, I. A., Ola, B., Hammadieh, N., Papaioannou, S., and Barratt, C. L. R. (2002). Critical evaluation of methylcellulose as an alternative medium in sperm migration tests. Hum. Reprod. 17, 143–149.
| Critical evaluation of methylcellulose as an alternative medium in sperm migration tests.Crossref | GoogleScholarGoogle Scholar |
Jikeli, J. F., Alvarez, L., Friedrich, B. M., Wilson, L. G., Pascal, R., Colin, R., Pichlo, M., Rennhack, A., Brenker, C., and Kaupp, U. B. (2015). Sperm navigation along helical paths in 3D chemoattractant landscapes. Nat. Commun. 6, 7985–7994.
| Sperm navigation along helical paths in 3D chemoattractant landscapes.Crossref | GoogleScholarGoogle Scholar |
Kanakasabapathy, M. K., Sadasivam, M., Singh, A., Preston, C., Thirumalaraju, P., Venkataraman, M., Bormann, C. L., Draz, M. S., Petrozza, J. C., and Shafiee, H. (2017). An automated smartphone-based diagnostic assay for point-of-care semen analysis. Sci. Transl. Med. 9, eaai7863.
| An automated smartphone-based diagnostic assay for point-of-care semen analysis.Crossref | GoogleScholarGoogle Scholar |
Katz, D. F., and Overstreet, J. W. (1981). Sperm motility assessment by videomicrography. Fertil. Steril. 35, 188–193.
| Sperm motility assessment by videomicrography.Crossref | GoogleScholarGoogle Scholar |
Kirkman-Brown, J. C., and Smith, D. J. (2011). Sperm motility: is viscosity fundamental to progress? Mol. Hum. Reprod. 17, 539–544.
| Sperm motility: is viscosity fundamental to progress?Crossref | GoogleScholarGoogle Scholar |
Lauga, E., and Powers, T. R. (2009). The hydrodynamics of swimming microorganisms. Rep. Prog. Phys. 72, 096601.
| The hydrodynamics of swimming microorganisms.Crossref | GoogleScholarGoogle Scholar |
Machin, K. E. (1958). Wave propagation along flagella. J. Exp. Biol. 35, 796–806.
Martinez, V. A., Besseling, R., Croze, O. A., Tailleur, J., Reufer, M., Schwarz-Linek, J., Wilson, L. G., Bees, M. A., and Poon, W. C. K. (2012). Differential dynamic microscopy: a high-throughput method for characterizing the motility of microorganisms. Biophys. J. 103, 1637–1647.
| Differential dynamic microscopy: a high-throughput method for characterizing the motility of microorganisms.Crossref | GoogleScholarGoogle Scholar |
Merola, F., Miccio, L., Memmolo, 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 |
Micó, V., Zalevsky, Z., Ferreira, C., and García, J. (2008). Superresolution digital holographic microscopy for three-dimensional samples. Opt. Express 16, 19260–19270.
| Superresolution digital holographic microscopy for three-dimensional samples.Crossref | GoogleScholarGoogle Scholar |
Miki, K., and Clapham, D. E. (2013). Rheotaxis guides mammalian sperm. Curr. Biol. 23, 443–452.
| Rheotaxis guides mammalian sperm.Crossref | GoogleScholarGoogle Scholar |
Mortimer, S. T., van der Horst, G., and Mortimer, D. (2015). The future of computer-aided sperm analysis. Asian J. Androl. 17, 545–553.
| The future of computer-aided sperm analysis.Crossref | GoogleScholarGoogle Scholar |
Ooi, E. H., Smith, D. J., Gadêlha, H., Gaffney, E. A., and Kirkman-Brown, J. C. (2014). The mechanics of hyperactivation in adhered human sperm. R. Soc. Open Sci. 1, 140230.
| The mechanics of hyperactivation in adhered human sperm.Crossref | GoogleScholarGoogle Scholar |
Pimentel, J. A., Carneiro, J., Darszon, A., and Corkidi, G. (2012). A segmentation algorithm for automated tracking of fast swimming unlabelled cells in three dimensions. J. Microsc. 245, 72–81.
| A segmentation algorithm for automated tracking of fast swimming unlabelled cells in three dimensions.Crossref | GoogleScholarGoogle Scholar |
Prokopchuk, G., and Cosson, J. (2017). Biophysics of fish sperm flagellar movement: present knowledge and original directions. In ‘Cytoskeleton – Structure, Dynamics, Function and Disease’. (Ed. J. C. Jimenez-Lopez.) Chapter 7. (InTech.) Available from: https://mts.intechopen.com/books/cytoskeleton-structure-dynamics-function-and-disease/biophysics-of-fish-sperm-flagellar-movement-present-knowledge-and-original-directions [verified 28 February 2018].
Purcell, E. M. (1977). Life at low Reynolds number. Am. J. Phys. 45, 3–11.
| Life at low Reynolds number.Crossref | GoogleScholarGoogle Scholar |
Rijnders, S., Bolscher, J. G. M., McDonnell, J., and Vermeiden, J. P. W. (2007). Andrology lab corner: filling time of a lamellar capillary-filling semen analysis chamber is a rapid, precise, and accurate method to assess viscosity of seminal plasma. J. Androl. 28, 461–465.
| Andrology lab corner: filling time of a lamellar capillary-filling semen analysis chamber is a rapid, precise, and accurate method to assess viscosity of seminal plasma.Crossref | GoogleScholarGoogle Scholar |
Rothschild, L. (1963). Non-random distribution of bull spermatozoa in a drop of sperm suspension. Nature 198, 1221–1222.
| Non-random distribution of bull spermatozoa in a drop of sperm suspension.Crossref | GoogleScholarGoogle Scholar |
Sanders, D., Fensome-Rimmer, S., and Woodward, B. (2017). Uncertainty of measurement in andrology: UK best practice guideline from the Association of Biomedical Andrologists. Br. J. Biomed. Sci. 74, 157–162.
| Uncertainty of measurement in andrology: UK best practice guideline from the Association of Biomedical Andrologists.Crossref | GoogleScholarGoogle Scholar |
Silva-Villalobos, F., Pimentel, J. A., Darszon, A., and Corkidi, G. (2014). Imaging of the 3D dynamics of flagellar beating in human sperm. In ‘2014 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society’, 26–30 August 2014, Chicago, IL, USA. pp. 190–193. (IEEE: Chicago, IL, USA.)
Smith, D. J., Gaffney, E. A., Blake, J. R., and Kirkman-Brown, J. C. (2009a). Human sperm accumulation near surfaces: a simulation study. J. Fluid Mech. 621, 289–320.
| Human sperm accumulation near surfaces: a simulation study.Crossref | GoogleScholarGoogle Scholar |
Smith, D. J., Gaffney, E. A., Gadêlha, H., Kapur, N., and Kirkman-Brown, J. C. (2009b). 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 |
Storey, B. T. (2008). Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int. J. Dev. Biol. 52, 427–437.
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 |
Su, T.-W., Choi, I., Feng, J., Huang, K., McLeod, E., and Ozcan, A. (2013). Sperm trajectories form chiral ribbons. Sci. Rep. 3, 1664–1671.
| Sperm trajectories form chiral ribbons.Crossref | GoogleScholarGoogle Scholar |
Suarez, S. S. (2015). Gamete and zygote transport. In ‘Kobil and Neill’s Physiology of Reproduction’. (Eds T. M. Plant and A. Zeleznik.) pp. 197–232. (Academic Press: New York.)
Suarez, S. S., Katz, D. F., Owen, D. H., Andrew, J. B., and Powell, R. L. (1991). Evidence for the function of hyperactivated motility in sperm. Biol. Reprod. 44, 375–381.
| Evidence for the function of hyperactivated motility in sperm.Crossref | GoogleScholarGoogle Scholar |
Talarczyk-Desole, J., Berger, A., Taszarek-Hauke, G., Hauke, J., Pawelczyk, L., and Jedrzejczak, P. (2017). Manual vs. computer-assisted sperm analysis: can CASA replace manual assessment of human semen in clinical practice? Ginekol. Pol. 88, 56–60.
| Manual vs. computer-assisted sperm analysis: can CASA replace manual assessment of human semen in clinical practice?Crossref | GoogleScholarGoogle Scholar |
Tomlinson, M. J. (2016). Uncertainty of measurement and clinical value of semen analysis: has standardisation through professional guidelines helped or hindered progress? Andrology 4, 763–770.
| Uncertainty of measurement and clinical value of semen analysis: has standardisation through professional guidelines helped or hindered progress?Crossref | GoogleScholarGoogle Scholar |
Tomlinson, M. J., Pooley, K., Simpson, T., Newton, T., Hopkisson, J., Jayaprakasan, K., Jayaprakasan, R., Naeem, A., and Pridmore, A. (2010). Validation of a novel computer-assisted sperm analysis (CASA) system using multitarget-tracking algorithms. Fertil. Steril. 93, 1911–1920.
| Validation of a novel computer-assisted sperm analysis (CASA) system using multitarget-tracking algorithms.Crossref | GoogleScholarGoogle Scholar |
Tung, C.-K., Lin, C., Harvey, B., Fiore, A. G., Ardon, F., Wu, M., and Suarez, S. S. (2017). Fluid viscoelasticity promotes collective swimming of sperm. Sci. Rep. 7, 3152–3160.
| Fluid viscoelasticity promotes collective swimming of sperm.Crossref | GoogleScholarGoogle Scholar |
Tyler, A., and Rothschild, L. (1951). Metabolism of sea urchin spermatozoa and induced anaerobic motility in solutions of amino acids. Proc. Soc. Exp. Biol. Med. 76, 52–58.
| Metabolism of sea urchin spermatozoa and induced anaerobic motility in solutions of amino acids.Crossref | GoogleScholarGoogle Scholar |
van der Horst, G., and Sanchez, E. (2016). Tracking sperm movement in four dimensions and models for sperm functionality. J. Polish Soc. Androl. 3, 72–73.
van der Horst, G., Seier, J. V., Spinks, A. C., and Hendricks, S. (1999). The maturation of sperm motility in the epididymis and vas deferens of the vervet monkey, Cercopithecus aethiops. Int. J. Androl. 22, 197–207.
| The maturation of sperm motility in the epididymis and vas deferens of the vervet monkey, Cercopithecus aethiops.Crossref | GoogleScholarGoogle Scholar |
World Health Organization (WHO) (2010). ‘WHO Laboratory Manual for the Examination and Processing of Human Semen.’ 5th edn. (WHO: Geneva, Switzerland.)
Wolf, D. P., Blasco, L., Khan, M. A., and Litt, M. (1977). Human cervical mucus. II. Changes in viscoelasticity during the ovulatory menstrual cycle. Fertil. Steril. 28, 47–52.
| Human cervical mucus. II. Changes in viscoelasticity during the ovulatory menstrual cycle.Crossref | GoogleScholarGoogle Scholar |
Woolley, D. M. (2003). Motility of spermatozoa at surfaces. Reproduction 126, 259–270.
| Motility of spermatozoa at surfaces.Crossref | GoogleScholarGoogle Scholar |
Woolley, D. M., Crockett, R. F., Groom, W. D. I., and Revell, S. G. (2009). A study of synchronisation between the flagella of bull spermatozoa, with related observations. J. Exp. Biol. 212, 2215–2223.
| A study of synchronisation between the flagella of bull spermatozoa, with related observations.Crossref | GoogleScholarGoogle Scholar |
