Skip to main content
Log in

Quantitative analysis of sperm rheotaxis using a microfluidic device

  • Research Paper
  • Published:
Microfluidics and Nanofluidics Aims and scope Submit manuscript

Abstract

Quite puzzling issue in biology is how sperm cells are selected naturally where human sperm has to maintain a correct swimming behavior during the various stages of reproduction process. In nature, sperm has to compete a long journey from cervix to oocyte to stand a chance for fertilization. Although various guidance mechanisms such as chemical and thermal gradients are proposed previously, these mechanisms may only be relevant as sperm reaches very close to the oocyte. Rheotaxis, a phenomenon where sperm cells swim against the flow direction, is possibly the long-range sperm guidance mechanism for successful fertilization. A little is known quantitatively about how flow shear effects may help guide human sperm cells over long distances. Here, we have developed microfluidic devices to quantitatively investigate sperm rheotaxis at various physiological flow conditions. We observed that at certain flow rates sperm actively orient and swim against the flow. Sperm that exhibit positive rheotaxis show better motility and velocity than the control (no-flow condition), however, rheotaxis does not select sperm based on hyaluronic acid (HA) binding potential and morphology. Morphology and HA binding potential may not be a significant factor in sperm transport in natural sperm selection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aitken R, Bronson R, Smith T, De Iuliis G (2013a) The source and significance of DNA damage in human spermatozoa; a commentary on diagnostic strategies and straw man fallacies. Mol Hum Reprod 19:475–485

    Article  Google Scholar 

  • Aitken R et al (2013b) On methods for the detection of reactive oxygen species generation by human spermatozoa: analysis of the cellular responses to catechol oestrogen, lipid aldehyde, menadione and arachidonic acid. Andrology 1:192–205

    Article  Google Scholar 

  • Asghar W, El Assal R, Shafiee H, Anchan RM, Demirci U (2014a) Preserving human cells for regenerative, reproductive, and transfusion medicine. Biotechnol J 9:895–903

    Article  Google Scholar 

  • Asghar W et al (2014b) Selection of functional human sperm with higher DNA integrity and fewer reactive oxygen species. Adv Healthc Mater 3:1671–1679

    Article  Google Scholar 

  • Beck-Fruchter R, Shalev E, Weiss A (2016) Clinical benefit using sperm hyaluronic acid binding technique in ICSI cycles: a systematic review and meta-analysis. Reprod Biomed Online 32:286–298

    Article  Google Scholar 

  • Boivin J, Bunting L, Collins JA, Nygren KG (2007) International estimates of infertility prevalence and treatment-seeking: potential need and demand for infertility medical care. Hum Reprod 22:1506–1512

    Article  Google Scholar 

  • Boryshpolets S, Pérez-Cerezales S, Eisenbach M (2015) Behavioral mechanism of human sperm in thermotaxis: a role for hyperactivation. Hum Reprod 30:884–892

    Article  Google Scholar 

  • Bretherton F (1961) Rheotaxis of spermatozoa. Proc R Soc Lond B Biol Sci 153:490–502

    Article  Google Scholar 

  • Chen Y-A, Huang Z-W, Tsai F-S, Chen C-Y, Lin C-M, Wo AM (2011) Analysis of sperm concentration and motility in a microfluidic device. Microfluid Nanofluid 10:59–67

    Article  Google Scholar 

  • Chen C-Y et al (2013) Sperm quality assessment via separation sedimentation in a microfluidic device. Analyst 138:4967–4974

    Article  Google Scholar 

  • Chengala A, Hondzo M, Sheng J (2013) Microalga propels along vorticity direction in a shear flow. Phys Rev E 87:052704

    Article  Google Scholar 

  • Cheung LSL et al (2009) Detachment of captured cancer cells under flow acceleration in a bio-functionalized microchannel. Lab Chip 9:1721–1731

    Article  Google Scholar 

  • Chinnasamy T et al (2018) Guidance and self-sorting of active swimmers: 3D periodic arrays increase persistence length of human sperm selecting for the fittest. Adv Sci 5:1700531

    Article  Google Scholar 

  • Cho BS, Schuster TG, Zhu X, Chang D, Smith GD, Takayama S (2003) Passively driven integrated microfluidic system for separation of motile sperm. Anal Chem 75:1671–1675

    Article  Google Scholar 

  • Coarsey CT, Esiobu N, Narayanan R, Pavlovic M, Shafiee H, Asghar W (2017) Strategies in Ebola virus disease (EVD) diagnostics at the point of care. Crit Rev Microbiol 43:779–798

    Article  Google Scholar 

  • Cooper TG et al (2010) World Health Organization reference values for human semen characteristics. Hum Reprod Update 16:231–245

    Article  Google Scholar 

  • Dyer S (2009) International estimates on infertility prevalence and treatment seeking: potential need and demand for medical care. Hum Reprod 24:2379–2380

    Article  Google Scholar 

  • Eisenbach M, Giojalas LC (2006) Sperm guidance in mammals—an unpaved road to the egg. Nat Rev Mol Cell Biol 7:276–285

    Article  Google Scholar 

  • El-sherry T, Abdel-Ghani M, Abou-Khalil N, Elsayed M, Abdelgawad M (2017) Effect of pH on rheotaxis of bull sperm using microfluidics. Reprod Domest Anim 52:781–790

    Article  Google Scholar 

  • Fu HC, Powers TR, Stocker R (2012) Bacterial rheotaxis. Proc Natl Acad Sci 109:4780–4785

    Article  Google Scholar 

  • Gaffney E, Gadêlha H, Smith D, Blake J, Kirkman-Brown J (2011) Mammalian sperm motility: observation and theory. Annu Rev Fluid Mech 43:501–528

    Article  MathSciNet  Google Scholar 

  • Gatimel N, Moreau J, Parinaud J, Léandri R (2017) Sperm morphology: assessment, pathophysiology, clinical relevance, and state of the art in 2017. Andrology 5:845–862

    Article  Google Scholar 

  • Ghaleno LR, Valojerdi MR, Chehrazi M, Samani FS, Yazdi RS (2016) Hyaluronic acid binding assay is highly sensitive to select human spermatozoa with good progressive motility, morphology, and nuclear maturity. Gynecol Obstet Investig 81:244–250

    Article  Google Scholar 

  • Gillies EA, Cannon RM, Green RB, Pacey AA (2009) Hydrodynamic propulsion of human sperm. J Fluid Mech 625:445–474

    Article  MathSciNet  Google Scholar 

  • González-Marín C, Gosálvez J, Roy R (2012) Types, causes, detection and repair of DNA fragmentation in animal and human sperm cells. Int J Mol Sci 13:14026–14052

    Article  Google Scholar 

  • Huszar G, Ozenci CC, Cayli S, Zavaczki Z, Hansch E, Vigue L (2003) Hyaluronic acid binding by human sperm indicates cellular maturity, viability, and unreacted acrosomal status. Fertil Steril 79:1616–1624

    Article  Google Scholar 

  • Huszar G, Ozkavukcu S, Jakab A, Celik-Ozenci C, Sati GL, Cayli S (2006) Hyaluronic acid binding ability of human sperm reflects cellular maturity and fertilizing potential: selection of sperm for intracytoplasmic sperm injection. Curr Opin Obstet Gynecol 18:260–267

    Article  Google Scholar 

  • Huszar G, Jakab A, Sakkas D, Ozenci C-C, Cayli S, Delpiano E, Ozkavukcu S (2007) Fertility testing and ICSI sperm selection by hyaluronic acid binding: clinical and genetic aspects. Reprod Biomed Online 14:650–663

    Article  Google Scholar 

  • Ishikawa Y, Usui T, Yamashita M, Kanemori Y, Baba T (2016) Surfing and swimming of ejaculated sperm in the mouse oviduct 1. Biol Reprod 94:81–89

    Article  Google Scholar 

  • Ishimoto K, Gaffney EA (2015) Fluid flow and sperm guidance: a simulation study of hydrodynamic sperm rheotaxis. J R Soc Interface 12:20150172

    Article  Google Scholar 

  • Javanmard M, Babrzadeh F, Davis R (2010) Microfluidic force spectroscopy for characterization of biomolecular interactions with piconewton resolution. Appl Phys Lett 97:173704

    Article  Google Scholar 

  • Kanakasabapathy MK et al (2017) Rapid, label-free CD4 testing using a smartphone compatible device. Lab Chip 17:2910–2919

    Article  Google Scholar 

  • Kantsler V, Dunkel J, Blayney M, Goldstein RE (2014) Rheotaxis facilitates upstream navigation of mammalian sperm cells. Elife 3:e02403

    Article  Google Scholar 

  • Knowlton SM, Sadasivam M, Tasoglu S (2015) Microfluidics for sperm research. Trends Biotechnol 33:221–229

    Article  Google Scholar 

  • Kovac JR, Smith RP, Cajipe M, Lamb DJ, Lipshultz LI (2017) Men with a complete absence of normal sperm morphology exhibit high rates of success without assisted reproduction. Asian J Androl 19:39

    Google Scholar 

  • Kovacs P, Kovats T, Sajgo A, Szollosi J, Matyas S, Kaali SG (2011) The role of hyaluronic acid binding assay in choosing the fertilization method for patients undergoing IVF for unexplained infertility. J Assist Reprod Genet 28:49–54

    Article  Google Scholar 

  • Krüger TH, Haake P, Hartmann U, Schedlowski M, Exton MS (2002) Orgasm-induced prolactin secretion: feedback control of sexual drive? Neurosci Biobehav Rev 26:31–44

    Article  Google Scholar 

  • Larson-Cook KL, Brannian JD, Hansen KA, Kasperson KM, Aamold ET, Evenson DP (2003) Relationship between the outcomes of assisted reproductive techniques and sperm DNA fragmentation as measured by the sperm chromatin structure assay. Fertil Steril 80:895–902

    Article  Google Scholar 

  • Mascarenhas MN, Flaxman SR, Boerma T, Vanderpoel S, Stevens GA (2012) National, regional, and global trends in infertility prevalence since 1990: a systematic analysis of 277 health surveys. PLOS Med 9(12):1–12

    Article  Google Scholar 

  • Mathijssen AJ, Shendruk TN, Yeomans JM, Doostmohammadi A (2016) Upstream swimming in microbiological flows. Phys Rev Lett 116:028104

    Article  Google Scholar 

  • Miki K, Clapham DE (2013) Rheotaxis guides mammalian sperm. Curr Biol 23:443–452

    Article  Google Scholar 

  • Nosrati R, Vollmer M, Eamer L, San Gabriel MC, Zeidan K, Zini A, Sinton D (2014) Rapid selection of sperm with high DNA integrity. Lab Chip 14:1142–1150

    Article  Google Scholar 

  • Ombelet W, Cooke I, Dyer S, Serour G, Devroey P (2008) Infertility and the provision of infertility medical services in developing countries. Hum Reprod Update 14:605–621. https://doi.org/10.1093/humupd/dmn042

    Article  Google Scholar 

  • Parker GH (1931) The passage of sperms and of eggs through the oviducts in terrestrial vertebrates. Philos Trans R Soc Lond Ser B Contain Pap Biol Character 219:381–419

    Article  Google Scholar 

  • Pasqualotto FF, Sharma RK, Nelson DR, Thomas AJ Jr, Agarwal A (2000) Relationship between oxidative stress, semen characteristics, and clinical diagnosis in men undergoing infertility investigation. Fertil Steril 73:459–464

    Article  Google Scholar 

  • Pérez-Cerezales S, Boryshpolets S, Afanzar O, Brandis A, Nevo R, Kiss V, Eisenbach M (2015a) Involvement of opsins in mammalian sperm thermotaxis. Sci Rep 5:16146

    Article  Google Scholar 

  • Pérez-Cerezales S, Boryshpolets S, Eisenbach M (2015b) Behavioral mechanisms of mammalian sperm guidance. Asian J Androl 17:628

    Article  Google Scholar 

  • Rappa KL, Rodriguez HF, Hakkarainen GC, Anchan RM, Mutter GL, Asghar W (2016) Sperm processing for advanced reproductive technologies: where are we today? Biotechnol Adv 34:578–587

    Article  Google Scholar 

  • Riffell JA, Zimmer RK (2007) Sex and flow: the consequences of fluid shear for sperm–egg interactions. J Exp Biol 210:3644–3660

    Article  Google Scholar 

  • Seo D-b, Agca Y, Feng Z, Critser JK (2007) Development of sorting, aligning, and orienting motile sperm using microfluidic device operated by hydrostatic pressure. Microfluid Nanofluid 3:561–570

    Article  Google Scholar 

  • Sharma S, Zhuang R, Long M, Pavlovic M, Kang Y, Ilyas A, Asghar W (2018) Circulating tumor cell isolation, culture, and downstream molecular analysis. Biotechnol Adv 36:1063–1078

    Article  Google Scholar 

  • Swain J, Lai D, Takayama S, Smith G (2013) Thinking big by thinking small: application of microfluidic technology to improve ART. Lab Chip 13:1213–1224

    Article  Google Scholar 

  • Tarozzi N, Nadalini M, Bizzaro D, Serrao L, Fava L, Scaravelli G, Borini A (2009) Sperm–hyaluronan-binding assay: clinical value in conventional IVF under Italian law. Reprod Biomed Online 19:35–43

    Article  Google Scholar 

  • Tasoglu S et al (2013) Exhaustion of racing sperm in nature-mimicking microfluidic channels during sorting. Small 9:3374–3384. https://doi.org/10.1002/smll.201300020

    Article  Google Scholar 

  • Tung C-k, Ardon F, Fiore AG, Suarez SS, Wu M (2014) Cooperative roles of biological flow and surface topography in guiding sperm migration revealed by a microfluidic model. Lab Chip 14:1348–1356

    Article  Google Scholar 

  • Wan Y, Tan J, Asghar W, Kim Y-t, Liu Y, Iqbal SM (2011) Velocity effect on aptamer-based circulating tumor cell isolation in microfluidic devices. J Phys Chem B 115:13891–13896

    Article  Google Scholar 

  • World Health Organization (2010) Laboratory manual for the examination and processing of human semen. World Health Organization, Geneva

    Google Scholar 

  • Worrilow K et al (2013) Use of hyaluronan in the selection of sperm for intracytoplasmic sperm injection (ICSI): significant improvement in clinical outcomes—multicenter, double-blinded and randomized controlled trial. Hum Reprod 28:306–314

    Article  Google Scholar 

  • Xie L et al (2010) Integration of sperm motility and chemotaxis screening with a microchannel-based device. Clin Chem 56:1270–1278

    Article  Google Scholar 

  • Yu S, Rubin M, Geevarughese S, Pino J, Rodriguez H, Asghar W (2018) Emerging technologies for home-based semen analysis. Andrology 6:10–19

    Article  Google Scholar 

  • Zhang Z, Liu J, Meriano J, Ru C, Xie S, Luo J, Sun Y (2016) Human sperm rheotaxis: a passive physical process. Sci Rep 6:23553

    Article  Google Scholar 

  • Zimmer RK, Riffell JA (2011) Sperm chemotaxis, fluid shear, and the evolution of sexual reproduction. Proc Natl Acad Sci 108:13200–13205

    Article  Google Scholar 

Download references

Acknowledgements

We acknowledge research support from Fertility and Genetics Plantation, FL, Cryos International USA, Institute for Sensing and Embedded Networking Systems Engineering (I-SENSE) Research Initiative Award, FAU Faculty Mentoring Award, Humanity in Science Award, and a start-up research support from College of Engineering and Computer Science, Florida Atlantic University, Boca Raton, FL.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Waseem Asghar.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 103 KB)

Supplementary material 2 (MP4 8753 KB)

Supplementary material 3 (MP4 7108 KB)

Supplementary material 4 (MP4 9652 KB)

Supplementary material 5 (MP4 9794 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rappa, K., Samargia, J., Sher, M. et al. Quantitative analysis of sperm rheotaxis using a microfluidic device. Microfluid Nanofluid 22, 100 (2018). https://doi.org/10.1007/s10404-018-2117-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10404-018-2117-6

Keywords

Navigation