Abstract

A 3D living-cell culture in hydrogel has been developed as a standardized low-tensile-strength tissue proxy for study of ultrafast, pulsetrain-burst laser-tissue interactions. The hydrogel is permeable to fluorescent biomarkers and optically transparent, allowing viable and necrotic cells to be imaged in 3D by confocal microscopy. Good cell-viability allowed us to distinguish between typical cell mortality and delayed subcellular tissue damage (e.g., apoptosis and DNA repair complex formation), caused by laser irradiation. The range of necrosis depended on laser intensity, but not on pulsetrain-burst duration. DNA double-strand breaks were quantified, giving a preliminary upper limit for genetic damage following laser treatment.

© 2013 Optical Society of America

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2013 (2)

G. Sutton, S. J. Bali, and C. Hodge, “Femtosecond cataract surgery: transitioning to laser cataract,” Curr. Opin. Ophthalmol.24(1), 3–8 (2013).
[CrossRef] [PubMed]

F. Schelle, S. Polz, H. Haloui, A. Braun, C. Dehn, M. Frentzen, and J. Meister, “Ultrashort pulsed laser (USPL) application in dentistry: basic investigations of ablation rates and thresholds on oral hard tissue and restorative materials,” Laser Med. Sci.2013, 1–9 (2013)

2012 (6)

C. L. Hoy, W. N. Everett, M. Yildirim, J. Kobler, S. M. Zeitels, and A. Ben-Yakar, “Towards endoscopic ultrafast laser microsurgery of vocal folds,” J. Biomed. Opt.17(3), 038002 (2012).
[CrossRef] [PubMed]

D. D. Lo, M. A. Mackanos, M. T. Chung, J. S. Hyun, D. T. Montoro, M. Grova, C. J. Liu, J. Wang, D. Palanker, A. J. Connolly, M. T. Longaker, C. H. Contag, and D. C. Wan, “Femtosecond plasma mediated laser ablation has advantages over mechanical osteotomy of cranial bone,” Lasers Surg. Med.44(10), 805–814 (2012).
[CrossRef] [PubMed]

K. R. Shull, “Materials Science: A Hard Concept in Soft Matter,” Nature489(7414), 36–37 (2012).
[CrossRef] [PubMed]

J. Y. Sun, X. H. Zhao, W. R. K. Illeperuma, O. Chaudhuri, K. H. Oh, D. J. Mooney, J. J. Vlassak, and Z. G. Suo, “Highly stretchable and tough hydrogels,” Nature489(7414), 133–136 (2012).
[CrossRef] [PubMed]

R. Marjoribanks, C. Dille, J. E. Schoenly, L. McKinney, A. G. Mordovanakis, P. Kaifosh, P. Forrester, Z. Qian, A. Covarrubias, Y. Feng, and L. Lilge, “Ablation and thermal effects in treatment of hard and soft materials and biotissues using ultrafast-laser pulse-train bursts,” Photon. Lasers Med.1(3), 155–169 (2012).
[CrossRef]

N. Tinne, E. Lubking, H. Lubatschowski, A. Kruger, and T. Ripken, “The influence of a spatial and temporal pulse-overlap on the laser-tissue-interaction of modern ophthalmic laser systems,” Biomed. Tech.57(Suppl 1),302–305 (2012)

2011 (9)

R. Gauvin, R. Parenteau-Bareil, D. Larouche, H. Marcoux, F. Bisson, A. Bonnet, F. A. Auger, S. Bolduc, and L. Germain, “Dynamic mechanical stimulations induce anisotropy and improve the tensile properties of engineered tissues produced without exogenous scaffolding,” Acta Biomater.7(9), 3294–3301 (2011).
[CrossRef] [PubMed]

J. S. D’Souza, J. A. Dharmadhikari, A. K. Dharmadhikari, B. J. Rao, and D. Mathur, “Effect of Intense, Ultrashort Laser Pulses on DNA Plasmids in their Native State: Strand Breakages Induced by In Situ Electrons and Radicals,” Phys. Rev. Lett.106(11), 118101 (2011).
[CrossRef] [PubMed]

M. F. Ali, “Topical delivery and photodynamic evaluation of a multivesicular liposomal Rose Bengal,” Lasers Med. Sci.26(2), 267–275 (2011).
[CrossRef] [PubMed]

C. Sramek, L. S. Leung, T. Leng, J. Brown, Y. M. Paulus, G. Schuele, and D. Palanker, “Improving the therapeutic window of retinal photocoagulation by spatial and temporal modulation of the laser beam,” J. Biomed. Opt.16(2), 028004 (2011).
[CrossRef] [PubMed]

F. Xu, J. Celli, I. Rizvi, S. Moon, T. Hasan, and U. Demirci, “A three-dimensional in vitro ovarian cancer coculture model using a high-throughput cell patterning platform,” Biotechnol. J.6(2), 204–212 (2011).
[CrossRef] [PubMed]

F. G. Pérez-Gutiérrez, S. Camacho-López, and G. Aguilar, “Time-resolved study of the mechanical response of tissue phantoms to nanosecond laser pulses,” J. Biomed. Opt.16(11), 115001 (2011).
[CrossRef] [PubMed]

P. Kim, G. L. Sutton, and D. S. Rootman, “Applications of the femtosecond laser in corneal refractive surgery,” Curr. Opin. Ophthalmol.22(4), 238–244 (2011).
[CrossRef] [PubMed]

K. Kuetemeyer, G. Kensah, M. Heidrich, H. Meyer, U. Martin, I. Gruh, and A. Heisterkamp, “Two-photon induced collagen cross-linking in bioartificial cardiac tissue,” Opt. Express19(17), 15996–16007 (2011).
[CrossRef] [PubMed]

V. Nuzzo, I. Maxwell, S. Chung, E. Mazur, and A. Heisterkamp, “Subcellular Surgery and Nanoneurosurgery Using Femtosecond Laser Pulses,” Nato. Sci. Peace Sec. B.2011, 203–218 (2011)

2010 (1)

H. C. Yalcin, A. Shekhar, N. Nishimura, A. A. Rane, C. B. Schaffer, and J. T. Butcher, “Two-photon microscopy-guided femtosecond-laser photoablation of avian cardiogenesis: noninvasive creation of localized heart defects,” Am. J. Physiol. Heart Circ. Physiol.299(5), H1728–H1735 (2010).
[CrossRef] [PubMed]

2009 (4)

R. G. McCaughey, H. Sun, V. S. Rothholtz, T. Juhasz, and B. J. F. Wong, “Femtosecond laser ablation of the stapes,” J. Biomed. Opt.14(2), 024040 (2009).
[CrossRef] [PubMed]

P. S. Tsai, P. Blinder, B. J. Migliori, J. Neev, Y. Jin, J. A. Squier, and D. Kleinfeld, “Plasma-mediated ablation: an optical tool for submicrometer surgery on neuronal and vascular systems,” Curr. Opin. Biotechnol.20(1), 90–99 (2009).
[CrossRef] [PubMed]

B. V. Slaughter, S. S. Khurshid, O. Z. Fisher, A. Khademhosseini, and N. A. Peppas, “Hydrogels in Regenerative Medicine,” Adv. Mater.21(32-33), 3307–3329 (2009).
[CrossRef] [PubMed]

M. A. El-Brawany, D. K. Nassiri, G. Terhaar, A. Shaw, I. Rivens, and K. Lozhken, “Measurement of thermal and ultrasonic properties of some biological tissues,” J. Med. Eng. Technol.33(3), 249–256 (2009).
[CrossRef] [PubMed]

2008 (1)

A. V. Cherian and K. R. Rau, “Pulsed-laser-induced damage in rat corneas: time-resolved imaging of physical effects and acute biological response,” J. Biomed. Opt.13(2), 024009 (2008).
[CrossRef] [PubMed]

2007 (1)

Y. Gong, L. He, J. Li, Q. Zhou, Z. Ma, C. Gao, and J. Shen, “Hydrogel-filled polylactide porous scaffolds for cartilage tissue engineering,” J. Biomed. Mater. Res. B Appl. Biomater.82B(1), 192–204 (2007).
[CrossRef] [PubMed]

2006 (2)

R. R. Gattass, L. R. Cerami, and E. Mazur, “Micromachining of bulk glass with bursts of femtosecond laser pulses at variable repetition rates,” Opt. Express14(12), 5279–5284 (2006).
[CrossRef] [PubMed]

R. R. Anderson, W. Farinelli, H. Laubach, D. Manstein, A. N. Yaroslavsky, J. Gubeli, K. Jordan, G. R. Neil, M. Shinn, W. Chandler, G. P. Williams, S. V. Benson, D. R. Douglas, and H. F. Dylla, “Selective photothermolysis of lipid-rich tissues: a free electron laser study,” Lasers Surg. Med.38(10), 913–919 (2006).
[CrossRef] [PubMed]

2005 (2)

L. McKinney, F. Frank, D. Graper, J. Dean, P. Forrester, M. Rioblanc, M. Nantel, and R. Marjoribanks, “Mitigating Intrinsic Defects and Laser Damage using Pulsetrain-burst (>100 MHZ) Ultrafast Laser Processing,” Proc. SPIE5970,14 (2005).

A. Vogel, J. Noack, G. Huttman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B81(8), 1015–1047 (2005).
[CrossRef]

2004 (2)

D. Manstein, G. S. Herron, R. K. Sink, H. Tanner, and R. R. Anderson, “Fractional photothermolysis: A new concept for cutaneous remodeling using microscopic patterns of thermal injury,” Lasers Surg. Med.34(5), 426–438 (2004).
[CrossRef] [PubMed]

N. K. Simha, C. S. Carlson, and J. L. Lewis, “Evaluation of fracture toughness of cartilage by micropenetration,” J. Mater. Sci. Mater. Med.15(5), 631–639 (2004).
[CrossRef] [PubMed]

2003 (4)

J. P. Gong, Y. Katsuyama, T. Kurokawa, and Y. Osada, “Double-network hydrogels with extremely high mechanical strength,” Adv. Mater.15(14), 1155–1158 (2003)

J. L. Drury and D. J. Mooney, “Hydrogels for tissue engineering: scaffold design variables and applications,” Biomaterials24(24), 4337–4351 (2003).
[CrossRef] [PubMed]

A. Vogel and V. Venugopalan, “Mechanisms of pulsed laser ablation of biological tissues,” Chem. Rev.103(2), 577–644 (2003).
[CrossRef] [PubMed]

I. Ratkay-Traub, I. E. Ferincz, T. Juhasz, R. M. Kurtz, and R. R. Krueger, “First clinical results with the femtosecond neodynium-glass laser in refractive surgery,” J. Refract. Surg.19(2), 94–103 (2003).
[PubMed]

2000 (1)

V. Normand, D. L. Lootens, E. Amici, K. P. Plucknett, and P. Aymard, “New insight into agarose gel mechanical properties,” Biomacromolecules1(4), 730–738 (2000).
[CrossRef] [PubMed]

1999 (2)

T. Juhasz, H. Frieder, R. M. Kurtz, C. Horvath, J. F. Bille, and G. Mourou, “Corneal refractive surgery with femtosecond lasers,” IEEE J. Sel. Top. Quantum Electron.5(4), 902–910 (1999).
[CrossRef]

P. R. Herman, A. Oettl, K. P. Chen, and R. S. Marjoribanks, “Laser micromachining of 'transparent' fused silica with 1-ps pulses and pulse trains,” Comm. Biomed. Appl. Ultrafast Lasers.3616, 148–155 (1999).
[CrossRef]

1998 (1)

E. P. Rogakou, D. R. Pilch, A. H. Orr, V. S. Ivanova, and W. M. Bonner, “DNA Double-stranded Breaks Induce Histone H2AX Phosphorylation on Serine 139,” J. Biol. Chem.273(10), 5858–5868 (1998).
[CrossRef] [PubMed]

1994 (2)

M. H. Niemz, “Investigation and Spectral-Analysis of the Plasma-Induced Ablation Mechanism of Dental Hydroxyapatite,” Appl. Phys. B58(4), 273–281 (1994).
[CrossRef]

G. Edwards, R. Logan, M. Copeland, L. Reinisch, J. Davidson, B. Johnson, R. Maciunas, M. Mendenhall, R. Ossoff, J. Tribble, J. Werkhaven, and D. O’Day, “Tissue ablation by a free-electron laser tuned to the amide II band,” Nature371(6496), 416–419 (1994).
[CrossRef] [PubMed]

1993 (1)

L. Reinisch and R. H. Ossoff, “Plasma ablation of hard tissue by the free-electron laser,” Proc. SPIE1854145 (1993).

1987 (1)

R. Mocharla, H. Mocharla, and M. E. Hodes, “A novel, sensitive fluorometric staining technique for the detection of DNA in RNA preparations,” Nucleic Acids Res.15(24), 10589 (1987).
[CrossRef] [PubMed]

1965 (1)

M. J. Waring, “Complex Formation between Ethidium Bromide and Nucleic Acids,” J. Mol. Biol.13(1), 269–282 (1965).
[CrossRef] [PubMed]

Aguilar, G.

F. G. Pérez-Gutiérrez, S. Camacho-López, and G. Aguilar, “Time-resolved study of the mechanical response of tissue phantoms to nanosecond laser pulses,” J. Biomed. Opt.16(11), 115001 (2011).
[CrossRef] [PubMed]

Ali, M. F.

M. F. Ali, “Topical delivery and photodynamic evaluation of a multivesicular liposomal Rose Bengal,” Lasers Med. Sci.26(2), 267–275 (2011).
[CrossRef] [PubMed]

Amici, E.

V. Normand, D. L. Lootens, E. Amici, K. P. Plucknett, and P. Aymard, “New insight into agarose gel mechanical properties,” Biomacromolecules1(4), 730–738 (2000).
[CrossRef] [PubMed]

Anderson, R. R.

R. R. Anderson, W. Farinelli, H. Laubach, D. Manstein, A. N. Yaroslavsky, J. Gubeli, K. Jordan, G. R. Neil, M. Shinn, W. Chandler, G. P. Williams, S. V. Benson, D. R. Douglas, and H. F. Dylla, “Selective photothermolysis of lipid-rich tissues: a free electron laser study,” Lasers Surg. Med.38(10), 913–919 (2006).
[CrossRef] [PubMed]

D. Manstein, G. S. Herron, R. K. Sink, H. Tanner, and R. R. Anderson, “Fractional photothermolysis: A new concept for cutaneous remodeling using microscopic patterns of thermal injury,” Lasers Surg. Med.34(5), 426–438 (2004).
[CrossRef] [PubMed]

Auger, F. A.

R. Gauvin, R. Parenteau-Bareil, D. Larouche, H. Marcoux, F. Bisson, A. Bonnet, F. A. Auger, S. Bolduc, and L. Germain, “Dynamic mechanical stimulations induce anisotropy and improve the tensile properties of engineered tissues produced without exogenous scaffolding,” Acta Biomater.7(9), 3294–3301 (2011).
[CrossRef] [PubMed]

Aymard, P.

V. Normand, D. L. Lootens, E. Amici, K. P. Plucknett, and P. Aymard, “New insight into agarose gel mechanical properties,” Biomacromolecules1(4), 730–738 (2000).
[CrossRef] [PubMed]

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G. Sutton, S. J. Bali, and C. Hodge, “Femtosecond cataract surgery: transitioning to laser cataract,” Curr. Opin. Ophthalmol.24(1), 3–8 (2013).
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R. R. Anderson, W. Farinelli, H. Laubach, D. Manstein, A. N. Yaroslavsky, J. Gubeli, K. Jordan, G. R. Neil, M. Shinn, W. Chandler, G. P. Williams, S. V. Benson, D. R. Douglas, and H. F. Dylla, “Selective photothermolysis of lipid-rich tissues: a free electron laser study,” Lasers Surg. Med.38(10), 913–919 (2006).
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C. L. Hoy, W. N. Everett, M. Yildirim, J. Kobler, S. M. Zeitels, and A. Ben-Yakar, “Towards endoscopic ultrafast laser microsurgery of vocal folds,” J. Biomed. Opt.17(3), 038002 (2012).
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Bille, J. F.

T. Juhasz, H. Frieder, R. M. Kurtz, C. Horvath, J. F. Bille, and G. Mourou, “Corneal refractive surgery with femtosecond lasers,” IEEE J. Sel. Top. Quantum Electron.5(4), 902–910 (1999).
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R. Gauvin, R. Parenteau-Bareil, D. Larouche, H. Marcoux, F. Bisson, A. Bonnet, F. A. Auger, S. Bolduc, and L. Germain, “Dynamic mechanical stimulations induce anisotropy and improve the tensile properties of engineered tissues produced without exogenous scaffolding,” Acta Biomater.7(9), 3294–3301 (2011).
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P. S. Tsai, P. Blinder, B. J. Migliori, J. Neev, Y. Jin, J. A. Squier, and D. Kleinfeld, “Plasma-mediated ablation: an optical tool for submicrometer surgery on neuronal and vascular systems,” Curr. Opin. Biotechnol.20(1), 90–99 (2009).
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R. Gauvin, R. Parenteau-Bareil, D. Larouche, H. Marcoux, F. Bisson, A. Bonnet, F. A. Auger, S. Bolduc, and L. Germain, “Dynamic mechanical stimulations induce anisotropy and improve the tensile properties of engineered tissues produced without exogenous scaffolding,” Acta Biomater.7(9), 3294–3301 (2011).
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E. P. Rogakou, D. R. Pilch, A. H. Orr, V. S. Ivanova, and W. M. Bonner, “DNA Double-stranded Breaks Induce Histone H2AX Phosphorylation on Serine 139,” J. Biol. Chem.273(10), 5858–5868 (1998).
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R. Gauvin, R. Parenteau-Bareil, D. Larouche, H. Marcoux, F. Bisson, A. Bonnet, F. A. Auger, S. Bolduc, and L. Germain, “Dynamic mechanical stimulations induce anisotropy and improve the tensile properties of engineered tissues produced without exogenous scaffolding,” Acta Biomater.7(9), 3294–3301 (2011).
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F. Schelle, S. Polz, H. Haloui, A. Braun, C. Dehn, M. Frentzen, and J. Meister, “Ultrashort pulsed laser (USPL) application in dentistry: basic investigations of ablation rates and thresholds on oral hard tissue and restorative materials,” Laser Med. Sci.2013, 1–9 (2013)

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C. Sramek, L. S. Leung, T. Leng, J. Brown, Y. M. Paulus, G. Schuele, and D. Palanker, “Improving the therapeutic window of retinal photocoagulation by spatial and temporal modulation of the laser beam,” J. Biomed. Opt.16(2), 028004 (2011).
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H. C. Yalcin, A. Shekhar, N. Nishimura, A. A. Rane, C. B. Schaffer, and J. T. Butcher, “Two-photon microscopy-guided femtosecond-laser photoablation of avian cardiogenesis: noninvasive creation of localized heart defects,” Am. J. Physiol. Heart Circ. Physiol.299(5), H1728–H1735 (2010).
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N. K. Simha, C. S. Carlson, and J. L. Lewis, “Evaluation of fracture toughness of cartilage by micropenetration,” J. Mater. Sci. Mater. Med.15(5), 631–639 (2004).
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F. Xu, J. Celli, I. Rizvi, S. Moon, T. Hasan, and U. Demirci, “A three-dimensional in vitro ovarian cancer coculture model using a high-throughput cell patterning platform,” Biotechnol. J.6(2), 204–212 (2011).
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Chandler, W.

R. R. Anderson, W. Farinelli, H. Laubach, D. Manstein, A. N. Yaroslavsky, J. Gubeli, K. Jordan, G. R. Neil, M. Shinn, W. Chandler, G. P. Williams, S. V. Benson, D. R. Douglas, and H. F. Dylla, “Selective photothermolysis of lipid-rich tissues: a free electron laser study,” Lasers Surg. Med.38(10), 913–919 (2006).
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J. Y. Sun, X. H. Zhao, W. R. K. Illeperuma, O. Chaudhuri, K. H. Oh, D. J. Mooney, J. J. Vlassak, and Z. G. Suo, “Highly stretchable and tough hydrogels,” Nature489(7414), 133–136 (2012).
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Chen, K. P.

P. R. Herman, A. Oettl, K. P. Chen, and R. S. Marjoribanks, “Laser micromachining of 'transparent' fused silica with 1-ps pulses and pulse trains,” Comm. Biomed. Appl. Ultrafast Lasers.3616, 148–155 (1999).
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A. V. Cherian and K. R. Rau, “Pulsed-laser-induced damage in rat corneas: time-resolved imaging of physical effects and acute biological response,” J. Biomed. Opt.13(2), 024009 (2008).
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D. D. Lo, M. A. Mackanos, M. T. Chung, J. S. Hyun, D. T. Montoro, M. Grova, C. J. Liu, J. Wang, D. Palanker, A. J. Connolly, M. T. Longaker, C. H. Contag, and D. C. Wan, “Femtosecond plasma mediated laser ablation has advantages over mechanical osteotomy of cranial bone,” Lasers Surg. Med.44(10), 805–814 (2012).
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Chung, S.

V. Nuzzo, I. Maxwell, S. Chung, E. Mazur, and A. Heisterkamp, “Subcellular Surgery and Nanoneurosurgery Using Femtosecond Laser Pulses,” Nato. Sci. Peace Sec. B.2011, 203–218 (2011)

Connolly, A. J.

D. D. Lo, M. A. Mackanos, M. T. Chung, J. S. Hyun, D. T. Montoro, M. Grova, C. J. Liu, J. Wang, D. Palanker, A. J. Connolly, M. T. Longaker, C. H. Contag, and D. C. Wan, “Femtosecond plasma mediated laser ablation has advantages over mechanical osteotomy of cranial bone,” Lasers Surg. Med.44(10), 805–814 (2012).
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D. D. Lo, M. A. Mackanos, M. T. Chung, J. S. Hyun, D. T. Montoro, M. Grova, C. J. Liu, J. Wang, D. Palanker, A. J. Connolly, M. T. Longaker, C. H. Contag, and D. C. Wan, “Femtosecond plasma mediated laser ablation has advantages over mechanical osteotomy of cranial bone,” Lasers Surg. Med.44(10), 805–814 (2012).
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Copeland, M.

G. Edwards, R. Logan, M. Copeland, L. Reinisch, J. Davidson, B. Johnson, R. Maciunas, M. Mendenhall, R. Ossoff, J. Tribble, J. Werkhaven, and D. O’Day, “Tissue ablation by a free-electron laser tuned to the amide II band,” Nature371(6496), 416–419 (1994).
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J. S. D’Souza, J. A. Dharmadhikari, A. K. Dharmadhikari, B. J. Rao, and D. Mathur, “Effect of Intense, Ultrashort Laser Pulses on DNA Plasmids in their Native State: Strand Breakages Induced by In Situ Electrons and Radicals,” Phys. Rev. Lett.106(11), 118101 (2011).
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G. Edwards, R. Logan, M. Copeland, L. Reinisch, J. Davidson, B. Johnson, R. Maciunas, M. Mendenhall, R. Ossoff, J. Tribble, J. Werkhaven, and D. O’Day, “Tissue ablation by a free-electron laser tuned to the amide II band,” Nature371(6496), 416–419 (1994).
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Dean, J.

L. McKinney, F. Frank, D. Graper, J. Dean, P. Forrester, M. Rioblanc, M. Nantel, and R. Marjoribanks, “Mitigating Intrinsic Defects and Laser Damage using Pulsetrain-burst (>100 MHZ) Ultrafast Laser Processing,” Proc. SPIE5970,14 (2005).

Dehn, C.

F. Schelle, S. Polz, H. Haloui, A. Braun, C. Dehn, M. Frentzen, and J. Meister, “Ultrashort pulsed laser (USPL) application in dentistry: basic investigations of ablation rates and thresholds on oral hard tissue and restorative materials,” Laser Med. Sci.2013, 1–9 (2013)

Demirci, U.

F. Xu, J. Celli, I. Rizvi, S. Moon, T. Hasan, and U. Demirci, “A three-dimensional in vitro ovarian cancer coculture model using a high-throughput cell patterning platform,” Biotechnol. J.6(2), 204–212 (2011).
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J. S. D’Souza, J. A. Dharmadhikari, A. K. Dharmadhikari, B. J. Rao, and D. Mathur, “Effect of Intense, Ultrashort Laser Pulses on DNA Plasmids in their Native State: Strand Breakages Induced by In Situ Electrons and Radicals,” Phys. Rev. Lett.106(11), 118101 (2011).
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Dharmadhikari, J. A.

J. S. D’Souza, J. A. Dharmadhikari, A. K. Dharmadhikari, B. J. Rao, and D. Mathur, “Effect of Intense, Ultrashort Laser Pulses on DNA Plasmids in their Native State: Strand Breakages Induced by In Situ Electrons and Radicals,” Phys. Rev. Lett.106(11), 118101 (2011).
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R. Marjoribanks, C. Dille, J. E. Schoenly, L. McKinney, A. G. Mordovanakis, P. Kaifosh, P. Forrester, Z. Qian, A. Covarrubias, Y. Feng, and L. Lilge, “Ablation and thermal effects in treatment of hard and soft materials and biotissues using ultrafast-laser pulse-train bursts,” Photon. Lasers Med.1(3), 155–169 (2012).
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R. R. Anderson, W. Farinelli, H. Laubach, D. Manstein, A. N. Yaroslavsky, J. Gubeli, K. Jordan, G. R. Neil, M. Shinn, W. Chandler, G. P. Williams, S. V. Benson, D. R. Douglas, and H. F. Dylla, “Selective photothermolysis of lipid-rich tissues: a free electron laser study,” Lasers Surg. Med.38(10), 913–919 (2006).
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J. L. Drury and D. J. Mooney, “Hydrogels for tissue engineering: scaffold design variables and applications,” Biomaterials24(24), 4337–4351 (2003).
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R. R. Anderson, W. Farinelli, H. Laubach, D. Manstein, A. N. Yaroslavsky, J. Gubeli, K. Jordan, G. R. Neil, M. Shinn, W. Chandler, G. P. Williams, S. V. Benson, D. R. Douglas, and H. F. Dylla, “Selective photothermolysis of lipid-rich tissues: a free electron laser study,” Lasers Surg. Med.38(10), 913–919 (2006).
[CrossRef] [PubMed]

Edwards, G.

G. Edwards, R. Logan, M. Copeland, L. Reinisch, J. Davidson, B. Johnson, R. Maciunas, M. Mendenhall, R. Ossoff, J. Tribble, J. Werkhaven, and D. O’Day, “Tissue ablation by a free-electron laser tuned to the amide II band,” Nature371(6496), 416–419 (1994).
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M. A. El-Brawany, D. K. Nassiri, G. Terhaar, A. Shaw, I. Rivens, and K. Lozhken, “Measurement of thermal and ultrasonic properties of some biological tissues,” J. Med. Eng. Technol.33(3), 249–256 (2009).
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C. L. Hoy, W. N. Everett, M. Yildirim, J. Kobler, S. M. Zeitels, and A. Ben-Yakar, “Towards endoscopic ultrafast laser microsurgery of vocal folds,” J. Biomed. Opt.17(3), 038002 (2012).
[CrossRef] [PubMed]

Farinelli, W.

R. R. Anderson, W. Farinelli, H. Laubach, D. Manstein, A. N. Yaroslavsky, J. Gubeli, K. Jordan, G. R. Neil, M. Shinn, W. Chandler, G. P. Williams, S. V. Benson, D. R. Douglas, and H. F. Dylla, “Selective photothermolysis of lipid-rich tissues: a free electron laser study,” Lasers Surg. Med.38(10), 913–919 (2006).
[CrossRef] [PubMed]

Feng, Y.

R. Marjoribanks, C. Dille, J. E. Schoenly, L. McKinney, A. G. Mordovanakis, P. Kaifosh, P. Forrester, Z. Qian, A. Covarrubias, Y. Feng, and L. Lilge, “Ablation and thermal effects in treatment of hard and soft materials and biotissues using ultrafast-laser pulse-train bursts,” Photon. Lasers Med.1(3), 155–169 (2012).
[CrossRef]

Ferincz, I. E.

I. Ratkay-Traub, I. E. Ferincz, T. Juhasz, R. M. Kurtz, and R. R. Krueger, “First clinical results with the femtosecond neodynium-glass laser in refractive surgery,” J. Refract. Surg.19(2), 94–103 (2003).
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B. V. Slaughter, S. S. Khurshid, O. Z. Fisher, A. Khademhosseini, and N. A. Peppas, “Hydrogels in Regenerative Medicine,” Adv. Mater.21(32-33), 3307–3329 (2009).
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R. Marjoribanks, C. Dille, J. E. Schoenly, L. McKinney, A. G. Mordovanakis, P. Kaifosh, P. Forrester, Z. Qian, A. Covarrubias, Y. Feng, and L. Lilge, “Ablation and thermal effects in treatment of hard and soft materials and biotissues using ultrafast-laser pulse-train bursts,” Photon. Lasers Med.1(3), 155–169 (2012).
[CrossRef]

L. McKinney, F. Frank, D. Graper, J. Dean, P. Forrester, M. Rioblanc, M. Nantel, and R. Marjoribanks, “Mitigating Intrinsic Defects and Laser Damage using Pulsetrain-burst (>100 MHZ) Ultrafast Laser Processing,” Proc. SPIE5970,14 (2005).

Frank, F.

L. McKinney, F. Frank, D. Graper, J. Dean, P. Forrester, M. Rioblanc, M. Nantel, and R. Marjoribanks, “Mitigating Intrinsic Defects and Laser Damage using Pulsetrain-burst (>100 MHZ) Ultrafast Laser Processing,” Proc. SPIE5970,14 (2005).

Frentzen, M.

F. Schelle, S. Polz, H. Haloui, A. Braun, C. Dehn, M. Frentzen, and J. Meister, “Ultrashort pulsed laser (USPL) application in dentistry: basic investigations of ablation rates and thresholds on oral hard tissue and restorative materials,” Laser Med. Sci.2013, 1–9 (2013)

Frieder, H.

T. Juhasz, H. Frieder, R. M. Kurtz, C. Horvath, J. F. Bille, and G. Mourou, “Corneal refractive surgery with femtosecond lasers,” IEEE J. Sel. Top. Quantum Electron.5(4), 902–910 (1999).
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Y. Gong, L. He, J. Li, Q. Zhou, Z. Ma, C. Gao, and J. Shen, “Hydrogel-filled polylactide porous scaffolds for cartilage tissue engineering,” J. Biomed. Mater. Res. B Appl. Biomater.82B(1), 192–204 (2007).
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Gauvin, R.

R. Gauvin, R. Parenteau-Bareil, D. Larouche, H. Marcoux, F. Bisson, A. Bonnet, F. A. Auger, S. Bolduc, and L. Germain, “Dynamic mechanical stimulations induce anisotropy and improve the tensile properties of engineered tissues produced without exogenous scaffolding,” Acta Biomater.7(9), 3294–3301 (2011).
[CrossRef] [PubMed]

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R. Gauvin, R. Parenteau-Bareil, D. Larouche, H. Marcoux, F. Bisson, A. Bonnet, F. A. Auger, S. Bolduc, and L. Germain, “Dynamic mechanical stimulations induce anisotropy and improve the tensile properties of engineered tissues produced without exogenous scaffolding,” Acta Biomater.7(9), 3294–3301 (2011).
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J. P. Gong, Y. Katsuyama, T. Kurokawa, and Y. Osada, “Double-network hydrogels with extremely high mechanical strength,” Adv. Mater.15(14), 1155–1158 (2003)

Gong, Y.

Y. Gong, L. He, J. Li, Q. Zhou, Z. Ma, C. Gao, and J. Shen, “Hydrogel-filled polylactide porous scaffolds for cartilage tissue engineering,” J. Biomed. Mater. Res. B Appl. Biomater.82B(1), 192–204 (2007).
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Graper, D.

L. McKinney, F. Frank, D. Graper, J. Dean, P. Forrester, M. Rioblanc, M. Nantel, and R. Marjoribanks, “Mitigating Intrinsic Defects and Laser Damage using Pulsetrain-burst (>100 MHZ) Ultrafast Laser Processing,” Proc. SPIE5970,14 (2005).

Grova, M.

D. D. Lo, M. A. Mackanos, M. T. Chung, J. S. Hyun, D. T. Montoro, M. Grova, C. J. Liu, J. Wang, D. Palanker, A. J. Connolly, M. T. Longaker, C. H. Contag, and D. C. Wan, “Femtosecond plasma mediated laser ablation has advantages over mechanical osteotomy of cranial bone,” Lasers Surg. Med.44(10), 805–814 (2012).
[CrossRef] [PubMed]

Gruh, I.

Gubeli, J.

R. R. Anderson, W. Farinelli, H. Laubach, D. Manstein, A. N. Yaroslavsky, J. Gubeli, K. Jordan, G. R. Neil, M. Shinn, W. Chandler, G. P. Williams, S. V. Benson, D. R. Douglas, and H. F. Dylla, “Selective photothermolysis of lipid-rich tissues: a free electron laser study,” Lasers Surg. Med.38(10), 913–919 (2006).
[CrossRef] [PubMed]

Haloui, H.

F. Schelle, S. Polz, H. Haloui, A. Braun, C. Dehn, M. Frentzen, and J. Meister, “Ultrashort pulsed laser (USPL) application in dentistry: basic investigations of ablation rates and thresholds on oral hard tissue and restorative materials,” Laser Med. Sci.2013, 1–9 (2013)

Hasan, T.

F. Xu, J. Celli, I. Rizvi, S. Moon, T. Hasan, and U. Demirci, “A three-dimensional in vitro ovarian cancer coculture model using a high-throughput cell patterning platform,” Biotechnol. J.6(2), 204–212 (2011).
[CrossRef] [PubMed]

He, L.

Y. Gong, L. He, J. Li, Q. Zhou, Z. Ma, C. Gao, and J. Shen, “Hydrogel-filled polylactide porous scaffolds for cartilage tissue engineering,” J. Biomed. Mater. Res. B Appl. Biomater.82B(1), 192–204 (2007).
[CrossRef] [PubMed]

Heidrich, M.

Heisterkamp, A.

K. Kuetemeyer, G. Kensah, M. Heidrich, H. Meyer, U. Martin, I. Gruh, and A. Heisterkamp, “Two-photon induced collagen cross-linking in bioartificial cardiac tissue,” Opt. Express19(17), 15996–16007 (2011).
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V. Nuzzo, I. Maxwell, S. Chung, E. Mazur, and A. Heisterkamp, “Subcellular Surgery and Nanoneurosurgery Using Femtosecond Laser Pulses,” Nato. Sci. Peace Sec. B.2011, 203–218 (2011)

Herman, P. R.

P. R. Herman, A. Oettl, K. P. Chen, and R. S. Marjoribanks, “Laser micromachining of 'transparent' fused silica with 1-ps pulses and pulse trains,” Comm. Biomed. Appl. Ultrafast Lasers.3616, 148–155 (1999).
[CrossRef]

Herron, G. S.

D. Manstein, G. S. Herron, R. K. Sink, H. Tanner, and R. R. Anderson, “Fractional photothermolysis: A new concept for cutaneous remodeling using microscopic patterns of thermal injury,” Lasers Surg. Med.34(5), 426–438 (2004).
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R. Mocharla, H. Mocharla, and M. E. Hodes, “A novel, sensitive fluorometric staining technique for the detection of DNA in RNA preparations,” Nucleic Acids Res.15(24), 10589 (1987).
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Hodge, C.

G. Sutton, S. J. Bali, and C. Hodge, “Femtosecond cataract surgery: transitioning to laser cataract,” Curr. Opin. Ophthalmol.24(1), 3–8 (2013).
[CrossRef] [PubMed]

Horvath, C.

T. Juhasz, H. Frieder, R. M. Kurtz, C. Horvath, J. F. Bille, and G. Mourou, “Corneal refractive surgery with femtosecond lasers,” IEEE J. Sel. Top. Quantum Electron.5(4), 902–910 (1999).
[CrossRef]

Hoy, C. L.

C. L. Hoy, W. N. Everett, M. Yildirim, J. Kobler, S. M. Zeitels, and A. Ben-Yakar, “Towards endoscopic ultrafast laser microsurgery of vocal folds,” J. Biomed. Opt.17(3), 038002 (2012).
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Huttman, G.

A. Vogel, J. Noack, G. Huttman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B81(8), 1015–1047 (2005).
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Hyun, J. S.

D. D. Lo, M. A. Mackanos, M. T. Chung, J. S. Hyun, D. T. Montoro, M. Grova, C. J. Liu, J. Wang, D. Palanker, A. J. Connolly, M. T. Longaker, C. H. Contag, and D. C. Wan, “Femtosecond plasma mediated laser ablation has advantages over mechanical osteotomy of cranial bone,” Lasers Surg. Med.44(10), 805–814 (2012).
[CrossRef] [PubMed]

Illeperuma, W. R. K.

J. Y. Sun, X. H. Zhao, W. R. K. Illeperuma, O. Chaudhuri, K. H. Oh, D. J. Mooney, J. J. Vlassak, and Z. G. Suo, “Highly stretchable and tough hydrogels,” Nature489(7414), 133–136 (2012).
[CrossRef] [PubMed]

Ivanova, V. S.

E. P. Rogakou, D. R. Pilch, A. H. Orr, V. S. Ivanova, and W. M. Bonner, “DNA Double-stranded Breaks Induce Histone H2AX Phosphorylation on Serine 139,” J. Biol. Chem.273(10), 5858–5868 (1998).
[CrossRef] [PubMed]

Jin, Y.

P. S. Tsai, P. Blinder, B. J. Migliori, J. Neev, Y. Jin, J. A. Squier, and D. Kleinfeld, “Plasma-mediated ablation: an optical tool for submicrometer surgery on neuronal and vascular systems,” Curr. Opin. Biotechnol.20(1), 90–99 (2009).
[CrossRef] [PubMed]

Johnson, B.

G. Edwards, R. Logan, M. Copeland, L. Reinisch, J. Davidson, B. Johnson, R. Maciunas, M. Mendenhall, R. Ossoff, J. Tribble, J. Werkhaven, and D. O’Day, “Tissue ablation by a free-electron laser tuned to the amide II band,” Nature371(6496), 416–419 (1994).
[CrossRef] [PubMed]

Jordan, K.

R. R. Anderson, W. Farinelli, H. Laubach, D. Manstein, A. N. Yaroslavsky, J. Gubeli, K. Jordan, G. R. Neil, M. Shinn, W. Chandler, G. P. Williams, S. V. Benson, D. R. Douglas, and H. F. Dylla, “Selective photothermolysis of lipid-rich tissues: a free electron laser study,” Lasers Surg. Med.38(10), 913–919 (2006).
[CrossRef] [PubMed]

Juhasz, T.

R. G. McCaughey, H. Sun, V. S. Rothholtz, T. Juhasz, and B. J. F. Wong, “Femtosecond laser ablation of the stapes,” J. Biomed. Opt.14(2), 024040 (2009).
[CrossRef] [PubMed]

I. Ratkay-Traub, I. E. Ferincz, T. Juhasz, R. M. Kurtz, and R. R. Krueger, “First clinical results with the femtosecond neodynium-glass laser in refractive surgery,” J. Refract. Surg.19(2), 94–103 (2003).
[PubMed]

T. Juhasz, H. Frieder, R. M. Kurtz, C. Horvath, J. F. Bille, and G. Mourou, “Corneal refractive surgery with femtosecond lasers,” IEEE J. Sel. Top. Quantum Electron.5(4), 902–910 (1999).
[CrossRef]

Kaifosh, P.

R. Marjoribanks, C. Dille, J. E. Schoenly, L. McKinney, A. G. Mordovanakis, P. Kaifosh, P. Forrester, Z. Qian, A. Covarrubias, Y. Feng, and L. Lilge, “Ablation and thermal effects in treatment of hard and soft materials and biotissues using ultrafast-laser pulse-train bursts,” Photon. Lasers Med.1(3), 155–169 (2012).
[CrossRef]

Katsuyama, Y.

J. P. Gong, Y. Katsuyama, T. Kurokawa, and Y. Osada, “Double-network hydrogels with extremely high mechanical strength,” Adv. Mater.15(14), 1155–1158 (2003)

Kensah, G.

Khademhosseini, A.

B. V. Slaughter, S. S. Khurshid, O. Z. Fisher, A. Khademhosseini, and N. A. Peppas, “Hydrogels in Regenerative Medicine,” Adv. Mater.21(32-33), 3307–3329 (2009).
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B. V. Slaughter, S. S. Khurshid, O. Z. Fisher, A. Khademhosseini, and N. A. Peppas, “Hydrogels in Regenerative Medicine,” Adv. Mater.21(32-33), 3307–3329 (2009).
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P. Kim, G. L. Sutton, and D. S. Rootman, “Applications of the femtosecond laser in corneal refractive surgery,” Curr. Opin. Ophthalmol.22(4), 238–244 (2011).
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P. S. Tsai, P. Blinder, B. J. Migliori, J. Neev, Y. Jin, J. A. Squier, and D. Kleinfeld, “Plasma-mediated ablation: an optical tool for submicrometer surgery on neuronal and vascular systems,” Curr. Opin. Biotechnol.20(1), 90–99 (2009).
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C. L. Hoy, W. N. Everett, M. Yildirim, J. Kobler, S. M. Zeitels, and A. Ben-Yakar, “Towards endoscopic ultrafast laser microsurgery of vocal folds,” J. Biomed. Opt.17(3), 038002 (2012).
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I. Ratkay-Traub, I. E. Ferincz, T. Juhasz, R. M. Kurtz, and R. R. Krueger, “First clinical results with the femtosecond neodynium-glass laser in refractive surgery,” J. Refract. Surg.19(2), 94–103 (2003).
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N. Tinne, E. Lubking, H. Lubatschowski, A. Kruger, and T. Ripken, “The influence of a spatial and temporal pulse-overlap on the laser-tissue-interaction of modern ophthalmic laser systems,” Biomed. Tech.57(Suppl 1),302–305 (2012)

Kuetemeyer, K.

Kurokawa, T.

J. P. Gong, Y. Katsuyama, T. Kurokawa, and Y. Osada, “Double-network hydrogels with extremely high mechanical strength,” Adv. Mater.15(14), 1155–1158 (2003)

Kurtz, R. M.

I. Ratkay-Traub, I. E. Ferincz, T. Juhasz, R. M. Kurtz, and R. R. Krueger, “First clinical results with the femtosecond neodynium-glass laser in refractive surgery,” J. Refract. Surg.19(2), 94–103 (2003).
[PubMed]

T. Juhasz, H. Frieder, R. M. Kurtz, C. Horvath, J. F. Bille, and G. Mourou, “Corneal refractive surgery with femtosecond lasers,” IEEE J. Sel. Top. Quantum Electron.5(4), 902–910 (1999).
[CrossRef]

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R. Gauvin, R. Parenteau-Bareil, D. Larouche, H. Marcoux, F. Bisson, A. Bonnet, F. A. Auger, S. Bolduc, and L. Germain, “Dynamic mechanical stimulations induce anisotropy and improve the tensile properties of engineered tissues produced without exogenous scaffolding,” Acta Biomater.7(9), 3294–3301 (2011).
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R. R. Anderson, W. Farinelli, H. Laubach, D. Manstein, A. N. Yaroslavsky, J. Gubeli, K. Jordan, G. R. Neil, M. Shinn, W. Chandler, G. P. Williams, S. V. Benson, D. R. Douglas, and H. F. Dylla, “Selective photothermolysis of lipid-rich tissues: a free electron laser study,” Lasers Surg. Med.38(10), 913–919 (2006).
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Leng, T.

C. Sramek, L. S. Leung, T. Leng, J. Brown, Y. M. Paulus, G. Schuele, and D. Palanker, “Improving the therapeutic window of retinal photocoagulation by spatial and temporal modulation of the laser beam,” J. Biomed. Opt.16(2), 028004 (2011).
[CrossRef] [PubMed]

Leung, L. S.

C. Sramek, L. S. Leung, T. Leng, J. Brown, Y. M. Paulus, G. Schuele, and D. Palanker, “Improving the therapeutic window of retinal photocoagulation by spatial and temporal modulation of the laser beam,” J. Biomed. Opt.16(2), 028004 (2011).
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N. K. Simha, C. S. Carlson, and J. L. Lewis, “Evaluation of fracture toughness of cartilage by micropenetration,” J. Mater. Sci. Mater. Med.15(5), 631–639 (2004).
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Y. Gong, L. He, J. Li, Q. Zhou, Z. Ma, C. Gao, and J. Shen, “Hydrogel-filled polylactide porous scaffolds for cartilage tissue engineering,” J. Biomed. Mater. Res. B Appl. Biomater.82B(1), 192–204 (2007).
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R. Marjoribanks, C. Dille, J. E. Schoenly, L. McKinney, A. G. Mordovanakis, P. Kaifosh, P. Forrester, Z. Qian, A. Covarrubias, Y. Feng, and L. Lilge, “Ablation and thermal effects in treatment of hard and soft materials and biotissues using ultrafast-laser pulse-train bursts,” Photon. Lasers Med.1(3), 155–169 (2012).
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D. D. Lo, M. A. Mackanos, M. T. Chung, J. S. Hyun, D. T. Montoro, M. Grova, C. J. Liu, J. Wang, D. Palanker, A. J. Connolly, M. T. Longaker, C. H. Contag, and D. C. Wan, “Femtosecond plasma mediated laser ablation has advantages over mechanical osteotomy of cranial bone,” Lasers Surg. Med.44(10), 805–814 (2012).
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D. D. Lo, M. A. Mackanos, M. T. Chung, J. S. Hyun, D. T. Montoro, M. Grova, C. J. Liu, J. Wang, D. Palanker, A. J. Connolly, M. T. Longaker, C. H. Contag, and D. C. Wan, “Femtosecond plasma mediated laser ablation has advantages over mechanical osteotomy of cranial bone,” Lasers Surg. Med.44(10), 805–814 (2012).
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G. Edwards, R. Logan, M. Copeland, L. Reinisch, J. Davidson, B. Johnson, R. Maciunas, M. Mendenhall, R. Ossoff, J. Tribble, J. Werkhaven, and D. O’Day, “Tissue ablation by a free-electron laser tuned to the amide II band,” Nature371(6496), 416–419 (1994).
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D. D. Lo, M. A. Mackanos, M. T. Chung, J. S. Hyun, D. T. Montoro, M. Grova, C. J. Liu, J. Wang, D. Palanker, A. J. Connolly, M. T. Longaker, C. H. Contag, and D. C. Wan, “Femtosecond plasma mediated laser ablation has advantages over mechanical osteotomy of cranial bone,” Lasers Surg. Med.44(10), 805–814 (2012).
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V. Normand, D. L. Lootens, E. Amici, K. P. Plucknett, and P. Aymard, “New insight into agarose gel mechanical properties,” Biomacromolecules1(4), 730–738 (2000).
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Lozhken, K.

M. A. El-Brawany, D. K. Nassiri, G. Terhaar, A. Shaw, I. Rivens, and K. Lozhken, “Measurement of thermal and ultrasonic properties of some biological tissues,” J. Med. Eng. Technol.33(3), 249–256 (2009).
[CrossRef] [PubMed]

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N. Tinne, E. Lubking, H. Lubatschowski, A. Kruger, and T. Ripken, “The influence of a spatial and temporal pulse-overlap on the laser-tissue-interaction of modern ophthalmic laser systems,” Biomed. Tech.57(Suppl 1),302–305 (2012)

Lubking, E.

N. Tinne, E. Lubking, H. Lubatschowski, A. Kruger, and T. Ripken, “The influence of a spatial and temporal pulse-overlap on the laser-tissue-interaction of modern ophthalmic laser systems,” Biomed. Tech.57(Suppl 1),302–305 (2012)

Ma, Z.

Y. Gong, L. He, J. Li, Q. Zhou, Z. Ma, C. Gao, and J. Shen, “Hydrogel-filled polylactide porous scaffolds for cartilage tissue engineering,” J. Biomed. Mater. Res. B Appl. Biomater.82B(1), 192–204 (2007).
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G. Edwards, R. Logan, M. Copeland, L. Reinisch, J. Davidson, B. Johnson, R. Maciunas, M. Mendenhall, R. Ossoff, J. Tribble, J. Werkhaven, and D. O’Day, “Tissue ablation by a free-electron laser tuned to the amide II band,” Nature371(6496), 416–419 (1994).
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D. D. Lo, M. A. Mackanos, M. T. Chung, J. S. Hyun, D. T. Montoro, M. Grova, C. J. Liu, J. Wang, D. Palanker, A. J. Connolly, M. T. Longaker, C. H. Contag, and D. C. Wan, “Femtosecond plasma mediated laser ablation has advantages over mechanical osteotomy of cranial bone,” Lasers Surg. Med.44(10), 805–814 (2012).
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R. R. Anderson, W. Farinelli, H. Laubach, D. Manstein, A. N. Yaroslavsky, J. Gubeli, K. Jordan, G. R. Neil, M. Shinn, W. Chandler, G. P. Williams, S. V. Benson, D. R. Douglas, and H. F. Dylla, “Selective photothermolysis of lipid-rich tissues: a free electron laser study,” Lasers Surg. Med.38(10), 913–919 (2006).
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R. Gauvin, R. Parenteau-Bareil, D. Larouche, H. Marcoux, F. Bisson, A. Bonnet, F. A. Auger, S. Bolduc, and L. Germain, “Dynamic mechanical stimulations induce anisotropy and improve the tensile properties of engineered tissues produced without exogenous scaffolding,” Acta Biomater.7(9), 3294–3301 (2011).
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L. McKinney, F. Frank, D. Graper, J. Dean, P. Forrester, M. Rioblanc, M. Nantel, and R. Marjoribanks, “Mitigating Intrinsic Defects and Laser Damage using Pulsetrain-burst (>100 MHZ) Ultrafast Laser Processing,” Proc. SPIE5970,14 (2005).

Marjoribanks, R. S.

P. R. Herman, A. Oettl, K. P. Chen, and R. S. Marjoribanks, “Laser micromachining of 'transparent' fused silica with 1-ps pulses and pulse trains,” Comm. Biomed. Appl. Ultrafast Lasers.3616, 148–155 (1999).
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Mathur, D.

J. S. D’Souza, J. A. Dharmadhikari, A. K. Dharmadhikari, B. J. Rao, and D. Mathur, “Effect of Intense, Ultrashort Laser Pulses on DNA Plasmids in their Native State: Strand Breakages Induced by In Situ Electrons and Radicals,” Phys. Rev. Lett.106(11), 118101 (2011).
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V. Nuzzo, I. Maxwell, S. Chung, E. Mazur, and A. Heisterkamp, “Subcellular Surgery and Nanoneurosurgery Using Femtosecond Laser Pulses,” Nato. Sci. Peace Sec. B.2011, 203–218 (2011)

Mazur, E.

V. Nuzzo, I. Maxwell, S. Chung, E. Mazur, and A. Heisterkamp, “Subcellular Surgery and Nanoneurosurgery Using Femtosecond Laser Pulses,” Nato. Sci. Peace Sec. B.2011, 203–218 (2011)

R. R. Gattass, L. R. Cerami, and E. Mazur, “Micromachining of bulk glass with bursts of femtosecond laser pulses at variable repetition rates,” Opt. Express14(12), 5279–5284 (2006).
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R. G. McCaughey, H. Sun, V. S. Rothholtz, T. Juhasz, and B. J. F. Wong, “Femtosecond laser ablation of the stapes,” J. Biomed. Opt.14(2), 024040 (2009).
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R. Marjoribanks, C. Dille, J. E. Schoenly, L. McKinney, A. G. Mordovanakis, P. Kaifosh, P. Forrester, Z. Qian, A. Covarrubias, Y. Feng, and L. Lilge, “Ablation and thermal effects in treatment of hard and soft materials and biotissues using ultrafast-laser pulse-train bursts,” Photon. Lasers Med.1(3), 155–169 (2012).
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L. McKinney, F. Frank, D. Graper, J. Dean, P. Forrester, M. Rioblanc, M. Nantel, and R. Marjoribanks, “Mitigating Intrinsic Defects and Laser Damage using Pulsetrain-burst (>100 MHZ) Ultrafast Laser Processing,” Proc. SPIE5970,14 (2005).

Meister, J.

F. Schelle, S. Polz, H. Haloui, A. Braun, C. Dehn, M. Frentzen, and J. Meister, “Ultrashort pulsed laser (USPL) application in dentistry: basic investigations of ablation rates and thresholds on oral hard tissue and restorative materials,” Laser Med. Sci.2013, 1–9 (2013)

Mendenhall, M.

G. Edwards, R. Logan, M. Copeland, L. Reinisch, J. Davidson, B. Johnson, R. Maciunas, M. Mendenhall, R. Ossoff, J. Tribble, J. Werkhaven, and D. O’Day, “Tissue ablation by a free-electron laser tuned to the amide II band,” Nature371(6496), 416–419 (1994).
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Migliori, B. J.

P. S. Tsai, P. Blinder, B. J. Migliori, J. Neev, Y. Jin, J. A. Squier, and D. Kleinfeld, “Plasma-mediated ablation: an optical tool for submicrometer surgery on neuronal and vascular systems,” Curr. Opin. Biotechnol.20(1), 90–99 (2009).
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R. Mocharla, H. Mocharla, and M. E. Hodes, “A novel, sensitive fluorometric staining technique for the detection of DNA in RNA preparations,” Nucleic Acids Res.15(24), 10589 (1987).
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D. D. Lo, M. A. Mackanos, M. T. Chung, J. S. Hyun, D. T. Montoro, M. Grova, C. J. Liu, J. Wang, D. Palanker, A. J. Connolly, M. T. Longaker, C. H. Contag, and D. C. Wan, “Femtosecond plasma mediated laser ablation has advantages over mechanical osteotomy of cranial bone,” Lasers Surg. Med.44(10), 805–814 (2012).
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F. Xu, J. Celli, I. Rizvi, S. Moon, T. Hasan, and U. Demirci, “A three-dimensional in vitro ovarian cancer coculture model using a high-throughput cell patterning platform,” Biotechnol. J.6(2), 204–212 (2011).
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J. L. Drury and D. J. Mooney, “Hydrogels for tissue engineering: scaffold design variables and applications,” Biomaterials24(24), 4337–4351 (2003).
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R. Marjoribanks, C. Dille, J. E. Schoenly, L. McKinney, A. G. Mordovanakis, P. Kaifosh, P. Forrester, Z. Qian, A. Covarrubias, Y. Feng, and L. Lilge, “Ablation and thermal effects in treatment of hard and soft materials and biotissues using ultrafast-laser pulse-train bursts,” Photon. Lasers Med.1(3), 155–169 (2012).
[CrossRef]

Mourou, G.

T. Juhasz, H. Frieder, R. M. Kurtz, C. Horvath, J. F. Bille, and G. Mourou, “Corneal refractive surgery with femtosecond lasers,” IEEE J. Sel. Top. Quantum Electron.5(4), 902–910 (1999).
[CrossRef]

Nantel, M.

L. McKinney, F. Frank, D. Graper, J. Dean, P. Forrester, M. Rioblanc, M. Nantel, and R. Marjoribanks, “Mitigating Intrinsic Defects and Laser Damage using Pulsetrain-burst (>100 MHZ) Ultrafast Laser Processing,” Proc. SPIE5970,14 (2005).

Nassiri, D. K.

M. A. El-Brawany, D. K. Nassiri, G. Terhaar, A. Shaw, I. Rivens, and K. Lozhken, “Measurement of thermal and ultrasonic properties of some biological tissues,” J. Med. Eng. Technol.33(3), 249–256 (2009).
[CrossRef] [PubMed]

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P. S. Tsai, P. Blinder, B. J. Migliori, J. Neev, Y. Jin, J. A. Squier, and D. Kleinfeld, “Plasma-mediated ablation: an optical tool for submicrometer surgery on neuronal and vascular systems,” Curr. Opin. Biotechnol.20(1), 90–99 (2009).
[CrossRef] [PubMed]

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R. R. Anderson, W. Farinelli, H. Laubach, D. Manstein, A. N. Yaroslavsky, J. Gubeli, K. Jordan, G. R. Neil, M. Shinn, W. Chandler, G. P. Williams, S. V. Benson, D. R. Douglas, and H. F. Dylla, “Selective photothermolysis of lipid-rich tissues: a free electron laser study,” Lasers Surg. Med.38(10), 913–919 (2006).
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M. H. Niemz, “Investigation and Spectral-Analysis of the Plasma-Induced Ablation Mechanism of Dental Hydroxyapatite,” Appl. Phys. B58(4), 273–281 (1994).
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H. C. Yalcin, A. Shekhar, N. Nishimura, A. A. Rane, C. B. Schaffer, and J. T. Butcher, “Two-photon microscopy-guided femtosecond-laser photoablation of avian cardiogenesis: noninvasive creation of localized heart defects,” Am. J. Physiol. Heart Circ. Physiol.299(5), H1728–H1735 (2010).
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Noack, J.

A. Vogel, J. Noack, G. Huttman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B81(8), 1015–1047 (2005).
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V. Normand, D. L. Lootens, E. Amici, K. P. Plucknett, and P. Aymard, “New insight into agarose gel mechanical properties,” Biomacromolecules1(4), 730–738 (2000).
[CrossRef] [PubMed]

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V. Nuzzo, I. Maxwell, S. Chung, E. Mazur, and A. Heisterkamp, “Subcellular Surgery and Nanoneurosurgery Using Femtosecond Laser Pulses,” Nato. Sci. Peace Sec. B.2011, 203–218 (2011)

O’Day, D.

G. Edwards, R. Logan, M. Copeland, L. Reinisch, J. Davidson, B. Johnson, R. Maciunas, M. Mendenhall, R. Ossoff, J. Tribble, J. Werkhaven, and D. O’Day, “Tissue ablation by a free-electron laser tuned to the amide II band,” Nature371(6496), 416–419 (1994).
[CrossRef] [PubMed]

Oettl, A.

P. R. Herman, A. Oettl, K. P. Chen, and R. S. Marjoribanks, “Laser micromachining of 'transparent' fused silica with 1-ps pulses and pulse trains,” Comm. Biomed. Appl. Ultrafast Lasers.3616, 148–155 (1999).
[CrossRef]

Oh, K. H.

J. Y. Sun, X. H. Zhao, W. R. K. Illeperuma, O. Chaudhuri, K. H. Oh, D. J. Mooney, J. J. Vlassak, and Z. G. Suo, “Highly stretchable and tough hydrogels,” Nature489(7414), 133–136 (2012).
[CrossRef] [PubMed]

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E. P. Rogakou, D. R. Pilch, A. H. Orr, V. S. Ivanova, and W. M. Bonner, “DNA Double-stranded Breaks Induce Histone H2AX Phosphorylation on Serine 139,” J. Biol. Chem.273(10), 5858–5868 (1998).
[CrossRef] [PubMed]

Osada, Y.

J. P. Gong, Y. Katsuyama, T. Kurokawa, and Y. Osada, “Double-network hydrogels with extremely high mechanical strength,” Adv. Mater.15(14), 1155–1158 (2003)

Ossoff, R.

G. Edwards, R. Logan, M. Copeland, L. Reinisch, J. Davidson, B. Johnson, R. Maciunas, M. Mendenhall, R. Ossoff, J. Tribble, J. Werkhaven, and D. O’Day, “Tissue ablation by a free-electron laser tuned to the amide II band,” Nature371(6496), 416–419 (1994).
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L. Reinisch and R. H. Ossoff, “Plasma ablation of hard tissue by the free-electron laser,” Proc. SPIE1854145 (1993).

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D. D. Lo, M. A. Mackanos, M. T. Chung, J. S. Hyun, D. T. Montoro, M. Grova, C. J. Liu, J. Wang, D. Palanker, A. J. Connolly, M. T. Longaker, C. H. Contag, and D. C. Wan, “Femtosecond plasma mediated laser ablation has advantages over mechanical osteotomy of cranial bone,” Lasers Surg. Med.44(10), 805–814 (2012).
[CrossRef] [PubMed]

C. Sramek, L. S. Leung, T. Leng, J. Brown, Y. M. Paulus, G. Schuele, and D. Palanker, “Improving the therapeutic window of retinal photocoagulation by spatial and temporal modulation of the laser beam,” J. Biomed. Opt.16(2), 028004 (2011).
[CrossRef] [PubMed]

Paltauf, G.

A. Vogel, J. Noack, G. Huttman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B81(8), 1015–1047 (2005).
[CrossRef]

Parenteau-Bareil, R.

R. Gauvin, R. Parenteau-Bareil, D. Larouche, H. Marcoux, F. Bisson, A. Bonnet, F. A. Auger, S. Bolduc, and L. Germain, “Dynamic mechanical stimulations induce anisotropy and improve the tensile properties of engineered tissues produced without exogenous scaffolding,” Acta Biomater.7(9), 3294–3301 (2011).
[CrossRef] [PubMed]

Paulus, Y. M.

C. Sramek, L. S. Leung, T. Leng, J. Brown, Y. M. Paulus, G. Schuele, and D. Palanker, “Improving the therapeutic window of retinal photocoagulation by spatial and temporal modulation of the laser beam,” J. Biomed. Opt.16(2), 028004 (2011).
[CrossRef] [PubMed]

Peppas, N. A.

B. V. Slaughter, S. S. Khurshid, O. Z. Fisher, A. Khademhosseini, and N. A. Peppas, “Hydrogels in Regenerative Medicine,” Adv. Mater.21(32-33), 3307–3329 (2009).
[CrossRef] [PubMed]

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F. G. Pérez-Gutiérrez, S. Camacho-López, and G. Aguilar, “Time-resolved study of the mechanical response of tissue phantoms to nanosecond laser pulses,” J. Biomed. Opt.16(11), 115001 (2011).
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E. P. Rogakou, D. R. Pilch, A. H. Orr, V. S. Ivanova, and W. M. Bonner, “DNA Double-stranded Breaks Induce Histone H2AX Phosphorylation on Serine 139,” J. Biol. Chem.273(10), 5858–5868 (1998).
[CrossRef] [PubMed]

Plucknett, K. P.

V. Normand, D. L. Lootens, E. Amici, K. P. Plucknett, and P. Aymard, “New insight into agarose gel mechanical properties,” Biomacromolecules1(4), 730–738 (2000).
[CrossRef] [PubMed]

Polz, S.

F. Schelle, S. Polz, H. Haloui, A. Braun, C. Dehn, M. Frentzen, and J. Meister, “Ultrashort pulsed laser (USPL) application in dentistry: basic investigations of ablation rates and thresholds on oral hard tissue and restorative materials,” Laser Med. Sci.2013, 1–9 (2013)

Qian, Z.

R. Marjoribanks, C. Dille, J. E. Schoenly, L. McKinney, A. G. Mordovanakis, P. Kaifosh, P. Forrester, Z. Qian, A. Covarrubias, Y. Feng, and L. Lilge, “Ablation and thermal effects in treatment of hard and soft materials and biotissues using ultrafast-laser pulse-train bursts,” Photon. Lasers Med.1(3), 155–169 (2012).
[CrossRef]

Rane, A. A.

H. C. Yalcin, A. Shekhar, N. Nishimura, A. A. Rane, C. B. Schaffer, and J. T. Butcher, “Two-photon microscopy-guided femtosecond-laser photoablation of avian cardiogenesis: noninvasive creation of localized heart defects,” Am. J. Physiol. Heart Circ. Physiol.299(5), H1728–H1735 (2010).
[CrossRef] [PubMed]

Rao, B. J.

J. S. D’Souza, J. A. Dharmadhikari, A. K. Dharmadhikari, B. J. Rao, and D. Mathur, “Effect of Intense, Ultrashort Laser Pulses on DNA Plasmids in their Native State: Strand Breakages Induced by In Situ Electrons and Radicals,” Phys. Rev. Lett.106(11), 118101 (2011).
[CrossRef] [PubMed]

Ratkay-Traub, I.

I. Ratkay-Traub, I. E. Ferincz, T. Juhasz, R. M. Kurtz, and R. R. Krueger, “First clinical results with the femtosecond neodynium-glass laser in refractive surgery,” J. Refract. Surg.19(2), 94–103 (2003).
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Rivens, I.

M. A. El-Brawany, D. K. Nassiri, G. Terhaar, A. Shaw, I. Rivens, and K. Lozhken, “Measurement of thermal and ultrasonic properties of some biological tissues,” J. Med. Eng. Technol.33(3), 249–256 (2009).
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F. Xu, J. Celli, I. Rizvi, S. Moon, T. Hasan, and U. Demirci, “A three-dimensional in vitro ovarian cancer coculture model using a high-throughput cell patterning platform,” Biotechnol. J.6(2), 204–212 (2011).
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E. P. Rogakou, D. R. Pilch, A. H. Orr, V. S. Ivanova, and W. M. Bonner, “DNA Double-stranded Breaks Induce Histone H2AX Phosphorylation on Serine 139,” J. Biol. Chem.273(10), 5858–5868 (1998).
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P. Kim, G. L. Sutton, and D. S. Rootman, “Applications of the femtosecond laser in corneal refractive surgery,” Curr. Opin. Ophthalmol.22(4), 238–244 (2011).
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R. G. McCaughey, H. Sun, V. S. Rothholtz, T. Juhasz, and B. J. F. Wong, “Femtosecond laser ablation of the stapes,” J. Biomed. Opt.14(2), 024040 (2009).
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H. C. Yalcin, A. Shekhar, N. Nishimura, A. A. Rane, C. B. Schaffer, and J. T. Butcher, “Two-photon microscopy-guided femtosecond-laser photoablation of avian cardiogenesis: noninvasive creation of localized heart defects,” Am. J. Physiol. Heart Circ. Physiol.299(5), H1728–H1735 (2010).
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Y. Gong, L. He, J. Li, Q. Zhou, Z. Ma, C. Gao, and J. Shen, “Hydrogel-filled polylactide porous scaffolds for cartilage tissue engineering,” J. Biomed. Mater. Res. B Appl. Biomater.82B(1), 192–204 (2007).
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D. Manstein, G. S. Herron, R. K. Sink, H. Tanner, and R. R. Anderson, “Fractional photothermolysis: A new concept for cutaneous remodeling using microscopic patterns of thermal injury,” Lasers Surg. Med.34(5), 426–438 (2004).
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C. Sramek, L. S. Leung, T. Leng, J. Brown, Y. M. Paulus, G. Schuele, and D. Palanker, “Improving the therapeutic window of retinal photocoagulation by spatial and temporal modulation of the laser beam,” J. Biomed. Opt.16(2), 028004 (2011).
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R. G. McCaughey, H. Sun, V. S. Rothholtz, T. Juhasz, and B. J. F. Wong, “Femtosecond laser ablation of the stapes,” J. Biomed. Opt.14(2), 024040 (2009).
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P. Kim, G. L. Sutton, and D. S. Rootman, “Applications of the femtosecond laser in corneal refractive surgery,” Curr. Opin. Ophthalmol.22(4), 238–244 (2011).
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G. Edwards, R. Logan, M. Copeland, L. Reinisch, J. Davidson, B. Johnson, R. Maciunas, M. Mendenhall, R. Ossoff, J. Tribble, J. Werkhaven, and D. O’Day, “Tissue ablation by a free-electron laser tuned to the amide II band,” Nature371(6496), 416–419 (1994).
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P. S. Tsai, P. Blinder, B. J. Migliori, J. Neev, Y. Jin, J. A. Squier, and D. Kleinfeld, “Plasma-mediated ablation: an optical tool for submicrometer surgery on neuronal and vascular systems,” Curr. Opin. Biotechnol.20(1), 90–99 (2009).
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R. R. Anderson, W. Farinelli, H. Laubach, D. Manstein, A. N. Yaroslavsky, J. Gubeli, K. Jordan, G. R. Neil, M. Shinn, W. Chandler, G. P. Williams, S. V. Benson, D. R. Douglas, and H. F. Dylla, “Selective photothermolysis of lipid-rich tissues: a free electron laser study,” Lasers Surg. Med.38(10), 913–919 (2006).
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R. G. McCaughey, H. Sun, V. S. Rothholtz, T. Juhasz, and B. J. F. Wong, “Femtosecond laser ablation of the stapes,” J. Biomed. Opt.14(2), 024040 (2009).
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H. C. Yalcin, A. Shekhar, N. Nishimura, A. A. Rane, C. B. Schaffer, and J. T. Butcher, “Two-photon microscopy-guided femtosecond-laser photoablation of avian cardiogenesis: noninvasive creation of localized heart defects,” Am. J. Physiol. Heart Circ. Physiol.299(5), H1728–H1735 (2010).
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Y. Gong, L. He, J. Li, Q. Zhou, Z. Ma, C. Gao, and J. Shen, “Hydrogel-filled polylactide porous scaffolds for cartilage tissue engineering,” J. Biomed. Mater. Res. B Appl. Biomater.82B(1), 192–204 (2007).
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C. Sramek, L. S. Leung, T. Leng, J. Brown, Y. M. Paulus, G. Schuele, and D. Palanker, “Improving the therapeutic window of retinal photocoagulation by spatial and temporal modulation of the laser beam,” J. Biomed. Opt.16(2), 028004 (2011).
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Phys. Rev. Lett. (1)

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Figures (6)

Fig. 1
Fig. 1

Experimental setup for pulsetrain-burst mode laser ablation experiments. The oscilloscope traces show that the N-pulse selector selects a portion of the burst from the oscillator. This selected burst is amplified by two four-pass amplifiers and focused onto the target. A 90:10 beam splitter (BS) directs part of the oncoming laser light to an energy monitor and part of the laser light reflected from the target to an equivalent target plane (CCD-ETP). Relevant lens focal lengths are shown in the image.

Fig. 2
Fig. 2

Comparing the number of intentionally insulted cells within the hydrogel to those in a naïve control hydrogel. (a) Cellular necrosis induced by heating with a hot water bath. (b) Cellular apoptosis induced by cis-platin. (c) DNA double-stranded breaks (DSBs) induced by an X-ray source at various dosages. The dimension listed near the top of each plot is the volume scanned by the confocal microscope.

Fig. 3
Fig. 3

The distribution of cells as a function of depth into the hydrogel, averaged over 4 field-of-views of 320µm × 320µm. (a) Cells tagged with Hoechst 33324 prior to seeding into the hydrogel. (b) Cells seeded into the hydrogel then tagged post facto with Hoechst 33342. (c) Necrotic cells within the hydrogel tagged post facto with PI. The cell count is relatively constant until a depth of ~700 μm from the hydrogel surface.

Fig. 4
Fig. 4

The normalized fluorescence intensity detected from various biomarkers as a function of depth into the hydrogel. Each set of data traces is normalized to the maximum intensity of each trace. The fluorescence data for cells tagged by PI, Annexin-V, and γH2AX is from the controlled insult experiments found in Fig. 2. Fluctuations in the fluorescence intensity with depth may reflect the inhomogeneity of marked cells within a given hydrogel sample.

Fig. 5
Fig. 5

(a) A lateral slice through an ablation crater in hydrogel as viewed under CFLSM. Voids at the crater edges are image artifacts, due to the steep edges of the crater. (b) The volume of the ablation crater in hydrogel as a function of per-pulse laser intensity at several pulsetrain burst durations.

Fig. 6
Fig. 6

(a) The number of viable and necrotic cells in hydrogel irradiated at a 4.6 × 1013-W/cm2 intensity and 1-μs-duration pulsetrain-burst as a function of distance from the centroid of the distribution of necrotic cells, but at the gel surface. Cells are binned in equal-volume, hemispherical shells. (b) Cylindrical projection of viable and necrotic cells, with hemispherical bins used for the analysis overlaid. The red hemisphere-line marks the necrosis range according to Gaussian fit. (c) The necrosis range as a function of the per-pulse laser intensity for a 1-μs-duration pulsetrain-burst. The line through the data points is a power-law fit with equation shown in the figure, where I 0 =1.0× 10 13 W/c m 2 , and C=138±28μm . Error bars on data points are standard deviations multiple of Gaussian fits using different total number of hemispherical shells. Data shown was taken over 5 days of experiments from 5 separately produced gels providing 21 punch-hole gel biopsies.

Tables (1)

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Table 1 The fracture stress and strain of 1% agarose hydrogel and various human biotissues.

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