Abstract

Assisted reproductive technologies seek to improve the success rate of pregnancies. Morphology scoring is a common approach to evaluate oocyte and embryo viability prior to embryo transfer in utero, but the efficacy of the method is low. We apply biodynamic imaging, based on dynamic light scattering and low-coherence digital holography, to assess the metabolic activity of oocytes and embryos. A biodynamic microscope, developed to image small and translucent biological specimens, is inserted into the bay of a commercial inverted microscope that can switch between conventional microscopy channels and biodynamic microscopy. We find intracellular Doppler spectral features that act as noninvasive proxies for embryo metabolic activity that may relate to embryo viability.

© 2020 Optical Society of America

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References

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2019 (3)

Z. Li, H. Sun, J. Turek, S. Jalal, M. Childress, and D. D. Nolte, “Doppler fluctuation spectroscopy of intracellular dynamics in living tissue,”J. Opt. Soc. Am. A 36, 665–677 (2019).
[Crossref]

Z. Li, N. Ehmke, I. M. Lorenzo, Z. Machaty, and D. Nolte, “Biodynamic optical assay for embryo viability,” J. Biomed. Opt. 24, 060502 (2019).
[Crossref]

H. Sasaki, T. Hamatan, S. Kamijo, M. Iwai, M. Kobanawa, S. Ogawa, and M. Tanaka, “Impact of oxidative stress on age-associated decline in oocyte developmental competence,” Front. Endocrinol. 10, 811 (2019).
[Crossref]

2018 (3)

H. Choi, Z. Li, H. Sun, D. Merrill, J. Turek, M. Childress, and D. Nolte, “Biodynamic digital holography of chemoresistance in a pre-clinical trial of canine B-cell lymphoma,” Biomed. Opt. Express 9, 2214–2228 (2018).
[Crossref]

V. Giorgione, F. Parazzini, V. Fesslova, S. Cipriani, M. Candiani, A. Inversetti, and P. Cavoretto, “Congenital heart defects in IVF/ICSI pregnancy: systematic review and meta-analysis,” Ultrasound Obstet. Gynecol. 51, 33–42 (2018).
[Crossref]

A. Busnelli and E. Somigliana, “Prognosis and cost-effectiveness of IVF in poor responders according to the bologna criteria,” Minerva Gynecol. 70, 89–98 (2018).
[Crossref]

2017 (2)

H. Sun, D. Merrill, R. An, J. Turek, D. Matei, and D. D. Nolte, “Biodynamic imaging for phenotypic profiling of three-dimensional tissue culture,” J. Biomed. Opt. 22, 016007 (2017).
[Crossref]

O. Thouvenin, C. Apelian, A. Nahas, M. Fink, and C. Boccara, “Full-field optical coherence tomography as a diagnosis tool: recent progress with multimodal imaging,” Appl. Sci. 7, 236 (2017).
[Crossref]

2016 (2)

D. Merrill, H. Sun, J. Turek, D. Nolte, B. Yakubov, D. Matei, and R. An, “Intracellular Doppler signatures of platinum sensitivity captured by biodynamic profiling in ovarian xenografts,” Sci. Rep. 6, 18821 (2016).
[Crossref]

H. Sudkamp, P. Koch, H. Spahr, D. Hillmann, G. Franke, M. Muenst, F. Reinholz, R. Birngruber, and G. Huettmann, “In-vivo retinal imaging with off-axis full-field time-domain optical coherence tomography,” Opt. Lett. 41, 4987–4990 (2016).
[Crossref]

2015 (3)

2014 (1)

R. An, D. Merrill, L. Avramova, J. Sturgis, M. Tsiper, J. P. Robinson, J. Turek, and D. D. Nolte, “Phenotypic profiling of Raf inhibitors and mitochondrial toxicity in 3D tissue using biodynamic Imaging,”J. Biomol. Screening 19, 526–537 (2014).
[Crossref]

2012 (2)

D. D. Nolte, R. An, J. Turek, and K. Jeong, “Tissue dynamics spectroscopy for phenotypic profiling of drug effects in three-dimensional culture,” Biomed. Opt. Express 3, 2825–2841 (2012).
[Crossref]

S. Ju and I. R. Ru, “Effects of cumulus cells on in vitro maturation of oocytes and development of cloned embryos in the pig,” Reprod. Domest. Anim. 47, 521–529 (2012).
[Crossref]

2011 (3)

J. E. Swain and G. D. Smith, “Advances in embryo culture platforms: novel approaches to improve preimplantation embryo development through modifications of the microenvironment,” Human Reprod. Update 17, 541–557 (2011).
[Crossref]

D. D. Nolte, R. An, J. Turek, and K. Jeong, “Holographic tissue dynamics spectroscopy,” J. Biomed. Opt. 16, 087004 (2011).
[Crossref]

M. Mills, R. R. Rindfuss, P. McDonald, and E. Te Velde, “Why do people postpone parenthood? reasons and social policy incentives,” Hum. Reprod. Update 17, 848–860 (2011).
[Crossref]

2010 (4)

T. Durduran, R. Choe, W. B. Baker, and A. G. Yodh, “Diffuse optics for tissue monitoring and tomography,” Rep. Prog. Phys. 73, 076701 (2010).
[Crossref]

K. Jeong, J. J. Turek, and D. D. Nolte, “Speckle fluctuation spectroscopy of intracellular motion in living tissue using coherence-domain digital holography,” J. Biomed. Opt. 15, 030514 (2010).
[Crossref]

N. T. Shaked, T. M. Newpher, M. D. Ehlers, and A. Wax, “Parallel on-axis holographic phase microscopy of biological cells and unicellular microorganism dynamics,” Appl. Opt. 49, 2872–2878 (2010).
[Crossref]

F. Hirschhaeuser, H. Menne, C. Dittfeld, J. West, W. Mueller-Klieser, and L. A. Kunz-Schughart, “Multicellular tumor spheroids: an underestimated tool is catching up again,” J. Biotechnol. 148, 3–15 (2010).
[Crossref]

2009 (1)

J. Friedrich, C. Seidel, R. Ebner, and L. A. Kunz-Schughart, “Spheroid-based drug screen: considerations and practical approach,” Nat. Protoc. 4, 309–324 (2009).
[Crossref]

2007 (2)

2006 (1)

B. Balaban and B. Urman, “Effect of oocyte morphology on embryo development and implantation,” Reprod. Biomed. Online 12, 608–615 (2006).
[Crossref]

2005 (3)

M. Cedars and R. B. Jaffe, “Infertility and women,” J. Clin. Endocrinol. Metab. 90, E2 (2005).
[Crossref]

B. Karamata, M. Leutenegger, M. Laubscher, S. Bourquin, T. Lasser, and P. Lambelet, “Multiple scattering in optical coherence tomography. II. Experimental and theoretical investigation of cross talk in wide-field optical coherence tomography,” J. Opt. Soc. Am. A 22, 1380–1388 (2005).
[Crossref]

A. Agarwal, S. Gupta, and R. K. Sharma, “Role of oxidative stress in female reproduction,” Reprod. Biol. Endocrinol. 3, 28 (2005).
[Crossref]

2004 (3)

L. A. Kunz-Schughart, J. P. Freyer, F. Hofstaedter, and R. Ebner, “The use of 3-D cultures for high-throughput screening: the multicellular spheroid model,” J. Biomol. Screening 9, 273–285 (2004).
[Crossref]

P. Yu, L. Peng, M. Mustata, J. J. Turek, M. R. Melloch, and D. D. Nolte, “Time-dependent speckle in holographic optical coherence Imaging and the state of health of tumor tissue,” Opt. Lett. 29, 68–70 (2004).
[Crossref]

A. Dubois, G. Moneron, K. Grieve, and A. C. Boccara, “Three-dimensional cellular-level imaging using full-field optical coherence tomography,” Phys. Med. Biol. 49, 1227–1234 (2004).
[Crossref]

2002 (2)

M. Alikani and S. M. Willadsen, “Human blastocysts from aggregated mononucleated cells of two or more non-viable zygote-derived embryos,” Reprod. Biomed. Online 5, 56–58 (2002).
[Crossref]

I. Boiso, A. Veiga, and R. G. Edwards, “Fundamentals of human embryonic growth in vitro and the selection of high-quality embryos for transfer,” Reprod. Biomed. Online 5, 328–350 (2002).
[Crossref]

2001 (3)

2000 (1)

B. Balaban, “Blastocyst quality affects the success of blastocyst-stage embryo transfer,” Fertil. Steril. 74, 282–287 (2000).
[Crossref]

1999 (1)

1998 (1)

K. K. Bizheva, A. M. Siegel, and D. A. Boas, “Path-length-resolved dynamic light scattering in highly scattering random media: the transition to diffusing wave spectroscopy,” Phys. Rev. E 58, 7664–7667 (1998).
[Crossref]

1996 (1)

H. Forsberg, H. L. Borg, E. Cagliero, and L. J. Eriksson, “Altered levels of scavenging enzymes in embryos subjected to a diabetic environment,” Free Radical Res. 24, 451–459 (1996).
[Crossref]

1995 (1)

D. A. Boas, L. E. Campbell, and A. G. Yodh, “Scattering and imaging with diffusing temporal field correlations,” Phys. Rev. Lett. 75, 1855–1858 (1995).
[Crossref]

1991 (1)

A. G. Yodh, N. Georgiades, and D. J. Pine, “Diffusing-wave interferometry,” Opt. Commun. 83, 56–59 (1991).
[Crossref]

1988 (1)

D. J. Pine, D. A. Weitz, P. M. Chaikin, and E. Herbolzheimer, “Diffusing-wave spectroscopy,” Phys. Rev. Lett. 60, 1134–1137 (1988).
[Crossref]

1987 (1)

R. B. Tishler and F. D. Carlson, “Quasi-Elastic light-scattering-studies of membrane motion in single red-blood-cells,” Biophys. J. 51, 993–997 (1987).
[Crossref]

1982 (1)

S. H. Chen and F. R. Hallett, “Determination of motile behavior of Prokaryotic and Eukaryotic cells by quasi-elastic light-scattering,” Q. Rev. Biophys. 15, 131–222 (1982).
[Crossref]

1981 (1)

V. A. Bloomfield, “Quasi-Elastic light-scattering applications in biochemistry and biology,” Annu. Rev. Biophys. Bioeng. 10, 421–450 (1981).
[Crossref]

1970 (1)

S. Fujime, “Quasi-Elastic light scattering from solutions of macromolecules. 2. Doppler broadening of light scattered from solutions of semi-flexible polymers, F-actin,” J. Phys. Soc. Jpn. 29, 751–759 (1970).
[Crossref]

Agarwal, A.

A. Agarwal, S. Gupta, and R. K. Sharma, “Role of oxidative stress in female reproduction,” Reprod. Biol. Endocrinol. 3, 28 (2005).
[Crossref]

Alabi, O.

Alikani, M.

M. Alikani and S. M. Willadsen, “Human blastocysts from aggregated mononucleated cells of two or more non-viable zygote-derived embryos,” Reprod. Biomed. Online 5, 56–58 (2002).
[Crossref]

An, R.

H. Sun, D. Merrill, R. An, J. Turek, D. Matei, and D. D. Nolte, “Biodynamic imaging for phenotypic profiling of three-dimensional tissue culture,” J. Biomed. Opt. 22, 016007 (2017).
[Crossref]

D. Merrill, H. Sun, J. Turek, D. Nolte, B. Yakubov, D. Matei, and R. An, “Intracellular Doppler signatures of platinum sensitivity captured by biodynamic profiling in ovarian xenografts,” Sci. Rep. 6, 18821 (2016).
[Crossref]

M. R. Custead, R. An, J. J. Turek, G. E. Moore, D. D. Nolte, and M. O. Childress, “Predictive value of ex vivo biodynamic imaging in determining response to chemotherapy in dogs with spontaneous non-Hodgkin’s lymphomas: a preliminary study,” Convergent Sci. Phys. Oncol. 1, 015003 (2015).
[Crossref]

R. An, C. Wang, J. Turek, Z. Machaty, and D. D. Nolte, “Biodynamic imaging of live porcine oocytes, zygotes and blastocysts for viability assessment in assisted reproductive technologies,” Biomed. Opt. Express 6, 963–976 (2015).
[Crossref]

R. An, D. Merrill, L. Avramova, J. Sturgis, M. Tsiper, J. P. Robinson, J. Turek, and D. D. Nolte, “Phenotypic profiling of Raf inhibitors and mitochondrial toxicity in 3D tissue using biodynamic Imaging,”J. Biomol. Screening 19, 526–537 (2014).
[Crossref]

D. D. Nolte, R. An, J. Turek, and K. Jeong, “Tissue dynamics spectroscopy for phenotypic profiling of drug effects in three-dimensional culture,” Biomed. Opt. Express 3, 2825–2841 (2012).
[Crossref]

D. D. Nolte, R. An, J. Turek, and K. Jeong, “Holographic tissue dynamics spectroscopy,” J. Biomed. Opt. 16, 087004 (2011).
[Crossref]

Ansari, Z.

Apelian, C.

O. Thouvenin, C. Apelian, A. Nahas, M. Fink, and C. Boccara, “Full-field optical coherence tomography as a diagnosis tool: recent progress with multimodal imaging,” Appl. Sci. 7, 236 (2017).
[Crossref]

Avramova, L.

R. An, D. Merrill, L. Avramova, J. Sturgis, M. Tsiper, J. P. Robinson, J. Turek, and D. D. Nolte, “Phenotypic profiling of Raf inhibitors and mitochondrial toxicity in 3D tissue using biodynamic Imaging,”J. Biomol. Screening 19, 526–537 (2014).
[Crossref]

Baker, W. B.

T. Durduran, R. Choe, W. B. Baker, and A. G. Yodh, “Diffuse optics for tissue monitoring and tomography,” Rep. Prog. Phys. 73, 076701 (2010).
[Crossref]

Balaban, B.

B. Balaban and B. Urman, “Effect of oocyte morphology on embryo development and implantation,” Reprod. Biomed. Online 12, 608–615 (2006).
[Crossref]

B. Balaban, “Blastocyst quality affects the success of blastocyst-stage embryo transfer,” Fertil. Steril. 74, 282–287 (2000).
[Crossref]

Bevilacqua, F.

Birngruber, R.

Bizheva, K. K.

K. K. Bizheva, A. M. Siegel, and D. A. Boas, “Path-length-resolved dynamic light scattering in highly scattering random media: the transition to diffusing wave spectroscopy,” Phys. Rev. E 58, 7664–7667 (1998).
[Crossref]

Bloomfield, V. A.

V. A. Bloomfield, “Quasi-Elastic light-scattering applications in biochemistry and biology,” Annu. Rev. Biophys. Bioeng. 10, 421–450 (1981).
[Crossref]

Boas, D. A.

K. K. Bizheva, A. M. Siegel, and D. A. Boas, “Path-length-resolved dynamic light scattering in highly scattering random media: the transition to diffusing wave spectroscopy,” Phys. Rev. E 58, 7664–7667 (1998).
[Crossref]

D. A. Boas, L. E. Campbell, and A. G. Yodh, “Scattering and imaging with diffusing temporal field correlations,” Phys. Rev. Lett. 75, 1855–1858 (1995).
[Crossref]

Boccara, A. C.

A. Dubois, G. Moneron, K. Grieve, and A. C. Boccara, “Three-dimensional cellular-level imaging using full-field optical coherence tomography,” Phys. Med. Biol. 49, 1227–1234 (2004).
[Crossref]

Boccara, C.

O. Thouvenin, C. Apelian, A. Nahas, M. Fink, and C. Boccara, “Full-field optical coherence tomography as a diagnosis tool: recent progress with multimodal imaging,” Appl. Sci. 7, 236 (2017).
[Crossref]

Boiso, I.

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D. Merrill, H. Sun, J. Turek, D. Nolte, B. Yakubov, D. Matei, and R. An, “Intracellular Doppler signatures of platinum sensitivity captured by biodynamic profiling in ovarian xenografts,” Sci. Rep. 6, 18821 (2016).
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Z. Li, N. Ehmke, I. M. Lorenzo, Z. Machaty, and D. Nolte, “Biodynamic optical assay for embryo viability,” J. Biomed. Opt. 24, 060502 (2019).
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H. Choi, Z. Li, H. Sun, D. Merrill, J. Turek, M. Childress, and D. Nolte, “Biodynamic digital holography of chemoresistance in a pre-clinical trial of canine B-cell lymphoma,” Biomed. Opt. Express 9, 2214–2228 (2018).
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Z. Li, H. Sun, J. Turek, S. Jalal, M. Childress, and D. D. Nolte, “Doppler fluctuation spectroscopy of intracellular dynamics in living tissue,”J. Opt. Soc. Am. A 36, 665–677 (2019).
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Parazzini, F.

V. Giorgione, F. Parazzini, V. Fesslova, S. Cipriani, M. Candiani, A. Inversetti, and P. Cavoretto, “Congenital heart defects in IVF/ICSI pregnancy: systematic review and meta-analysis,” Ultrasound Obstet. Gynecol. 51, 33–42 (2018).
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R. An, D. Merrill, L. Avramova, J. Sturgis, M. Tsiper, J. P. Robinson, J. Turek, and D. D. Nolte, “Phenotypic profiling of Raf inhibitors and mitochondrial toxicity in 3D tissue using biodynamic Imaging,”J. Biomol. Screening 19, 526–537 (2014).
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S. Ju and I. R. Ru, “Effects of cumulus cells on in vitro maturation of oocytes and development of cloned embryos in the pig,” Reprod. Domest. Anim. 47, 521–529 (2012).
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H. Sasaki, T. Hamatan, S. Kamijo, M. Iwai, M. Kobanawa, S. Ogawa, and M. Tanaka, “Impact of oxidative stress on age-associated decline in oocyte developmental competence,” Front. Endocrinol. 10, 811 (2019).
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J. Friedrich, C. Seidel, R. Ebner, and L. A. Kunz-Schughart, “Spheroid-based drug screen: considerations and practical approach,” Nat. Protoc. 4, 309–324 (2009).
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R. An, D. Merrill, L. Avramova, J. Sturgis, M. Tsiper, J. P. Robinson, J. Turek, and D. D. Nolte, “Phenotypic profiling of Raf inhibitors and mitochondrial toxicity in 3D tissue using biodynamic Imaging,”J. Biomol. Screening 19, 526–537 (2014).
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Z. Li, H. Sun, J. Turek, S. Jalal, M. Childress, and D. D. Nolte, “Doppler fluctuation spectroscopy of intracellular dynamics in living tissue,”J. Opt. Soc. Am. A 36, 665–677 (2019).
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J. E. Swain and G. D. Smith, “Advances in embryo culture platforms: novel approaches to improve preimplantation embryo development through modifications of the microenvironment,” Human Reprod. Update 17, 541–557 (2011).
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Te Velde, E.

M. Mills, R. R. Rindfuss, P. McDonald, and E. Te Velde, “Why do people postpone parenthood? reasons and social policy incentives,” Hum. Reprod. Update 17, 848–860 (2011).
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Figures (9)

Fig. 1.
Fig. 1. System setup of the BDM. (a) Photo of the BDM on a vibration isolation breadboard. (b) The BDI module that is inserted into the Olympus microscope. (c) 3D layout of the optical design of the BDI system. ${{\rm L}_1}$, Fourier transform lens with a focal length = 100 mm; ${{\rm L}_2}$, imaging lens with a focal length = 60 mm; ${{\rm L}_3}$, phase compensation lens. (d) Illustration of the 45º illumination. (e) Data flow showing the hologram, a selection of fringes, the Fourier transform to the image domain with two sidebands, and the extracted image for a cumulus-oocyte complex (COC) sample.
Fig. 2.
Fig. 2. Images of a multicellular tumor spheroid. (a) Conventional transillumination image. (b) Optical coherence image (OCI). (c) Motility contrast image (MCI). (d) MCI volumetric reconstruction of a DLD-1 tumor spheroid showing the necrotic region of the core surrounded by the proliferating shell. (e) BDM insert in the Olympus IX-73 inverted microscope. Scale bars are 100 µm.
Fig. 3.
Fig. 3. Spectral amplitudes of several types of biological samples measured on the BDI module of the BDM. The healthy sample is a day-four parthenogenetic embryo. The knee frequency of the healthy sample is 0.1 Hz representing an average intracellular speed of 40 nm/s. The azide sample is an embryo cultured in the presence of ${{\rm NaN}_3}$ to inhibit metabolism. The dead embryo was treated with glutaraldehyde (GA) to crosslink proteins in the sample and prevent most motion. The noise floor from a static target establishes the spectral noise floor of the BDM system.
Fig. 4.
Fig. 4. Averaged fluctuation spectra. (a) Spectra for healthy and azide-treated parthenotes. (b) Three-segment linear fitting for spectra. (Markers are a subset of data points with even intervals). Reprinted from [35].
Fig. 5.
Fig. 5. Effect of oocyte aging on biodynamic spectra and developmental potential. (a) Doppler fluctuation spectrum for day-two and day-three oocytes. The day-three samples are redshifted relative to day-two indicating lower metabolic activity. (b) Blastocyst development after seven days. A total of 195 oocytes were cultured after parthenogenetic activation to evaluate developmental potential of oocytes matured for two days (young oocytes; $n = {105}$) and those matured for three days (aged oocytes; $n = {90}$). The bars are standard errors.
Fig. 6.
Fig. 6. Biodynamic spectrograms of zygote formation. (a) Spectrogram of a zygote that developed a second polar body after fertilization. (b) Spectrogram of an unfertilized oocyte (no second polar body).
Fig. 7.
Fig. 7. Biodynamic markers associated with ATP concentrations. (a) Samples marked by their Nyquist floor and ${s_1}$ values and the proposed criteria for embryo selection. The ellipse of “high ATP” is one standard deviation from the average of the Nyquist floor and of the ${s_1}$ value of samples with the highest ATP content. (b) Receiver operator curve (ROC) of an SVM discriminator based on the principle component of an SVD analysis. The AUC = 0.74.
Fig. 8.
Fig. 8. Comparison of morphological grading to biodynamic features. (a) Boxplot of sample NSD, grouped by their grades. (b) Scatter plot of sample “$s$” and “NSD” biomarkers, grouped by their grades. While morphological features relate to structural characteristics, biodynamic features relate to functional characteristics. Structural and functional behavior are mostly independent.
Fig. 9.
Fig. 9. Comparison of transillumination microscopy, optical coherence imaging (OCI), and motility contrast imaging (MCI). (a) A representative day-four (8–16 cell stage) parthenote. (b) An IVF embryo. Scale bars are 50 µm. (c) Average spectra of IVF embryos compared with parthenotes.

Tables (3)

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Table 1. Specification of the BDM

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Table 2. Typical Values for Embryo Biodynamic Biomarkers

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Table 3. Morphological Grading

Equations (2)

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S = A / ω t ω 0 s t + ω s t + N y ,
D ( f ; t ) = log S ( f ; t ) log S ( f ; t 0 ) ,

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