Abstract

We demonstrate the utility of multimodal coherent anti-Stokes Raman scattering (CARS) microscopy for the study of structured condensed carbohydrate systems. Simultaneous second-harmonic generation (SHG) and spectrally-scanned CARS microscopy was used to elucidate structure, alignment, and density in cellulose cotton fibers and in starch grains undergoing rapid heat-moisture swelling. Our results suggest that CARS response of the O-H stretch region (3000 cm−1–3400 cm−1), together with the commonly-measured C-H stretch (2750 cm−1–2970 cm−1) and SHG provide potentially important structural information and contrast in these materials.

© 2010 Optical Society of America

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2010 (8)

A. F. Pegoraro, A. D. Slepkov, A. Ridsdale, J. P. Pezacki, A. Stolow, “Single laser source for multimodal coherent anti-Stokes Raman scattering microscopy,” Appl. Opt. 49(25), F10–F17 (2010).
[CrossRef] [PubMed]

R. S. Lim, A. Kratzer, N. P. Barry, S. Miyazaki-Anzai, M. Miyazaki, W. W. Mantulin, M. Levi, E. O. Potma, B. J. Tromberg, “Multimodal CARS microscopy determination of the impact of diet on macrophage infiltration and lipid accumulation on plaque formation in ApoE-deficient mice,” J. Lipid Res. 51(7), 1729–1737 (2010).
[CrossRef] [PubMed]

L. B. Mostaço-Guidolin, M. G. Sowa, A. Ridsdale, A. F. Pegoraro, M. S. D. Smith, M. D. Hewko, E. K. Kohlenberg, B. Schattka, M. Shiomi, A. Stolow, A. C.-T. Ko, “Differentiating atherosclerotic plaque burden in arterial tissues using femtosecond CARS-based multimodal nonlinear optical imaging,” Biomed. Opt. Express 1(1), 59–73 (2010).
[CrossRef]

S. Psilodimitrakopoulos, I. Amat-Roldan, P. Loza-Alvarez, D. Artigas, “Estimating the helical pitch angle of amylopectin in starch using polarization second harmonic generation microscopy,” J. Opt. 12(8), 084007 (2010).
[CrossRef]

Z.-Y. Zhuo, C.-S. Liao, C.-H. Huang, J.-Y. Yu, Y.-Y. Tzeng, W. Lo, C.-Y. Dong, H.-C. Chui, Y.-C. Huang, H.-M. Lai, S.-W. Chu, “Second harmonic generation imaging - a new method for unraveling molecular information of starch,” J. Struct. Biol. 171(1), 88–94 (2010).
[CrossRef] [PubMed]

B. Bakri, S. J. Eichhorn, “Elastic coils: deformation micromechanics of coir and celery fibres,” Cellulose 17(1), 1–11 (2010).
[CrossRef]

M. Zimmerley, R. Younger, T. Valenton, D. C. Oertel, J. L. Ward, E. O. Potma, “Molecular orientation in dry and hydrated cellulose fibers: a coherent anti-Stokes Raman scattering microscopy study,” J. Phys. Chem. B 114(31), 10200–10208 (2010).
[CrossRef] [PubMed]

N. Gierlinger, S. Luss, C. König, J. Konnerth, M. Eder, P. Fratzl, “Cellulose microfibril orientation of Picea abies and its variability at the micron-level determined by Raman imaging,” J. Exp. Bot. 61(2), 587–595 (2010).
[CrossRef] [PubMed]

2009 (4)

R. Cisek, L. Spencer, N. Prent, D. Zigmantas, G. S. Espie, V. Barzda, “Optical microscopy in photosynthesis,” Photosynth. Res. 102(2–3), 111–141 (2009).
[CrossRef] [PubMed]

R. Carriles, D. N. Schafer, K. E. Sheetz, J. J. Field, R. Cisek, V. Barzda, A. W. Sylvester, J. A. Squier, “Invited review article: Imaging techniques for harmonic and multiphoton absorption fluorescence microscopy,” Rev. Sci. Instrum. 80(8), 081101 (2009).
[CrossRef] [PubMed]

R. K. Lyn, D. C. Kennedy, S. M. Sagan, D. R. Blais, Y. Rouleau, A. F. Pegoraro, X. S. Xie, A. Stolow, J. P. Pezacki, “Direct imaging of the disruption of hepatitis C virus replication complexes by inhibitors of lipid metabolism,” Virology 394(1), 130–142 (2009).
[CrossRef] [PubMed]

A. F. Pegoraro, A. Ridsdale, D. J. Moffatt, Y. Jia, J. P. Pezacki, A. Stolow, “Optimally chirped multimodal CARS microscopy based on a single Ti:sapphire oscillator,” Opt. Express 17(4), 2984–2996 (2009).
[CrossRef] [PubMed]

2008 (6)

Y. Fu, T. B. Huff, H.-W. Wang, J.-X. Cheng, H. Wang, “Ex vivo and in vivo imaging of myelin fibers in mouse brain by coherent anti-Stokes Raman scattering microscopy,” Opt. Express 16(24), 19396–19409 (2008).
[CrossRef] [PubMed]

H.-W. Wang, T. T. Le, J.-X. Cheng, “Label-free imaging of arterial cells and extracellular matrix using a multimodal CARS microscope,” Opt. Commun. 281(7), 1813–1822 (2008).
[CrossRef] [PubMed]

C. W. Freudiger, W. Min, B. G. Saar, S. Lu, G. R. Holtom, C. He, J. C. Tsai, J. X. Kang, X. S. Xie, “Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy,” Science 322(5909), 1857–1861 (2008).
[CrossRef] [PubMed]

C. L. Evans, X. S. Xie, “Coherent anti-stokes Raman scattering microscopy: chemical imaging for biology and medicine,” Annu Rev Anal Chem (Palo Alto Calif) 1(1), 883–909 (2008).
[CrossRef] [PubMed]

K. N. Anisha Thayil, E. J. Gualda, S. Psilodimitrakopoulos, I. G. Cormack, I. Amat-Roldán, M. Mathew, D. Artigas, P. Loza-Alvarez, “Starch-based backwards SHG for in situ MEFISTO pulse characterization in multiphoton microscopy,” J. Microsc. 230(1), 70–75 (2008).
[CrossRef] [PubMed]

C. P. Pfeffer, B. R. Olsen, F. Ganikhanov, F. Légaré, “Multimodal nonlinear optical imaging of collagen arrays,” J. Struct. Biol. 164(1), 140–145 (2008).
[CrossRef] [PubMed]

2007 (5)

A. Buléon, G. Véronèse, J.-L. Putaux, “Self-association and crystallization of amylose,” Aust. J. Chem. 60(10), 706–718 (2007).
[CrossRef]

T. Loftsson, D. Duchêne, “Cyclodextrins and their pharmaceutical applications,” Int. J. Pharm. 329(1–2), 1–11 (2007).
[CrossRef] [PubMed]

T. Hellerer, C. Axäng, C. Brackmann, P. Hillertz, M. Pilon, A. Enejder, “Monitoring of lipid storage in Caenorhabditis elegans using coherent anti-Stokes Raman scattering (CARS) microscopy,” Proc. Natl. Acad. Sci. U.S.A. 104(37), 14658–14663 (2007).
[CrossRef] [PubMed]

M. E. Himmel, S. Y. Ding, D. K. Johnson, W. S. Adney, M. R. Nimlos, J. W. Brady, T. D. Foust, “Biomass recalcitrance: engineering plants and enzymes for biofuels production,” Science 315(5813), 804–807 (2007).
[CrossRef] [PubMed]

O. Nadiarnykh, R. B. Lacomb, P. J. Campagnola, W. A. Mohler, “Coherent and incoherent SHG in fibrillar cellulose matrices,” Opt. Express 15(6), 3348–3360 (2007).
[CrossRef] [PubMed]

2006 (2)

B. von Vacano, T. Buckup, M. Motzkus, “Highly sensitive single-beam heterodyne coherent anti-Stokes Raman scattering,” Opt. Lett. 31(16), 2495–2497 (2006).
[CrossRef] [PubMed]

X. Nan, E. O. Potma, X. S. Xie, “Nonperturbative chemical imaging of organelle transport in living cells with coherent anti-stokes Raman scattering microscopy,” Biophys. J. 91(2), 728–735 (2006).
[CrossRef] [PubMed]

2005 (5)

H. Wang, Y. Fu, P. Zickmund, R. Shi, J.-X. Cheng, “Coherent anti-stokes Raman scattering imaging of axonal myelin in live spinal tissues,” Biophys. J. 89(1), 581–591 (2005).
[CrossRef] [PubMed]

H. Wang, Y. Fu, P. Zickmund, R. Shi, J.-X. Cheng, “Coherent anti-stokes Raman scattering imaging of axonal myelin in live spinal tissues,” Biophys. J. 89(1), 581–591 (2005).
[CrossRef] [PubMed]

P. M. Fechner, S. Wartewig, P. Kleinebudde, R. H. Neubert, “Studies of the retrogradation process for various starch gels using Raman spectroscopy,” Carbohydr. Res. 340(16), 2563–2568 (2005).
[CrossRef] [PubMed]

G. Cox, N. Moreno, J. Feijó, “Second-harmonic imaging of plant polysaccharides,” J. Biomed. Opt. 10(2), 024013 (2005).
[CrossRef] [PubMed]

D. Klemm, B. Heublein, H. P. Fink, A. Bohn, “Cellulose: fascinating biopolymer and sustainable raw material,” Angew. Chem. Int. Ed. Engl. 44(22), 3358–3393 (2005).
[CrossRef] [PubMed]

2004 (4)

Y. Marubashi, T. Higashi, S. Hirakawa, S. Tani, T. Erata, M. Takai, J. Kawamata, “Second Harmonic Generaion Measurements for Biomacromolecules: Celluloses,” Opt. Rev. 11(6), 385–387 (2004).
[CrossRef]

M. Åkerholm, B. Hinterstoisser, L. Salmén, “Characterization of the crystalline structure of cellulose using static and dynamic FT-IR spectroscopy,” Carbohydr. Res. 339(3), 569–578 (2004).
[CrossRef] [PubMed]

T. Hellerer, A. M. K. Enejder, A. Zumbusch, “Spectral focusing: high spectral resolution spectroscopy with broad-bandwidth laser pulses,” Appl. Phys. Lett. 85, 25 (2004).
[CrossRef]

J.-X. Cheng, X. Xie, “Coherent anti-Stokes Raman scattering microscopy: Instrumentation, theory, and applications,” J. Phys. Chem. B 108(3), 827–840 (2004).
[CrossRef]

2003 (2)

E. O. Potma, X. S. Xie, “Detection of single lipid bilayers with coherent anti-Stokes Raman scattering (CARS) microscopy,” J. Raman Spectrosc. 34(9), 642–650 (2003).
[CrossRef]

R. M. J. Brown, A. C. Millard, P. J. Campagnola, “Macromolecular structure of cellulose studied by second-harmonic generation imaging microscopy,” Opt. Lett. 28(22), 2207–2209 (2003).
[CrossRef] [PubMed]

2002 (3)

M. Müller, J. M. Schins, “Imaging the thermodynamic state of lipid membranes with multiplex CARS microscopy,” J. Phys. Chem. B 106(14), 3715–3723 (2002).
[CrossRef]

J.-X. Cheng, A. Volkmer, L. D. Book, X. S. Xie, “Multiplex coherent anti-stokes Raman scattering microspectroscopy and study of lipid vesicles,” J. Phys. Chem. B 106(34), 8493–8498 (2002).
[CrossRef]

A. Gunaratne, R. Hoover, “Effect of heat-moisture treatment on the structure and physicochemical properties of tuber and root starches,” Carbohydr. Polym. 49(4), 425–437 (2002).
[CrossRef]

2001 (2)

J.-X. Cheng, L. D. Book, X. S. Xie, “Polarization coherent anti-Stokes Raman scattering microscopy,” Opt. Lett. 26(17), 1341–1343 (2001).
[CrossRef] [PubMed]

B. Hinterstoisser, M. Akerholm, L. Salmén, “Effect of fiber orientation in dynamic FTIR study on native cellulose,” Carbohydr. Res. 334(1), 27–37 (2001).
[CrossRef] [PubMed]

1999 (1)

A. Zumbusch, G. R. Holtom, X. S. Xie, “Three-dimensional vibrational imaging by coherent anti-Stokes Raman scattering,” Phys. Rev. Lett. 82(20), 4142–4145 (1999).
[CrossRef]

1997 (2)

T. T. Teeri, “Crystalline cellulose degredation: new insight into the function of cellobiohydrolases,” Trends Biotechnol. 15(5), 160–167 (1997).
[CrossRef]

D. J. Gallant, B. Bouchet, P. M. Baldwin, “Microscopy of starch: evidence of a new level of granule organization,” Carbohydr. Polym. 32(3–4), 177–191 (1997).
[CrossRef]

1991 (1)

C. G. Biliaderis, “The structure and interactions of starch with food constituents,” Can. J. Physiol. Pharmacol. 69(1), 60–78 (1991).
[PubMed]

1988 (1)

H. F. Zobel, “Molecules to Granules: A Comprehensive Starch Review,” Starch 4044–50 (1988).

1987 (1)

J. H. Wiley, R. H. Atalla, “Band assignments in the Raman-spectra of celluloses,” Carbohydr. Res. 160, 113–129 (1987).
[CrossRef]

Adney, W. S.

M. E. Himmel, S. Y. Ding, D. K. Johnson, W. S. Adney, M. R. Nimlos, J. W. Brady, T. D. Foust, “Biomass recalcitrance: engineering plants and enzymes for biofuels production,” Science 315(5813), 804–807 (2007).
[CrossRef] [PubMed]

Akerholm, M.

B. Hinterstoisser, M. Akerholm, L. Salmén, “Effect of fiber orientation in dynamic FTIR study on native cellulose,” Carbohydr. Res. 334(1), 27–37 (2001).
[CrossRef] [PubMed]

Åkerholm, M.

M. Åkerholm, B. Hinterstoisser, L. Salmén, “Characterization of the crystalline structure of cellulose using static and dynamic FT-IR spectroscopy,” Carbohydr. Res. 339(3), 569–578 (2004).
[CrossRef] [PubMed]

Amat-Roldan, I.

S. Psilodimitrakopoulos, I. Amat-Roldan, P. Loza-Alvarez, D. Artigas, “Estimating the helical pitch angle of amylopectin in starch using polarization second harmonic generation microscopy,” J. Opt. 12(8), 084007 (2010).
[CrossRef]

Amat-Roldán, I.

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Supplementary Material (2)

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Figures (5)

Fig. 1
Fig. 1

Femtosecond single-source multimodal CARS microscopy optical layout: Pulses from a Ti:Sapphire oscillator are sent through a prism compressor before being split by a variable beam splitter. One arm is sent through a photonic crystal fiber (PCF) where it generates a broadband supercontinuum Stokes light. This beam then passes to a long-pass (λ>900 nm) filter (LPF) and a 5-cm-long block of SF-6 before being recombined on a dichroic mirror (DM). The other beam is sent through a time delay arm and a variable attenuator. The two beams are recombined and then pass through an additional 10-cm of SF-6 glass before being routed into an Olympus FV300 microscope. The forward-propagating CARS and SHG signals are separated from the excitation pulses with a long-pass (λ<700 nm, SPF) filter (SPF), collected in a non-descanned geometry through a multimode fiber and are routed to off-board detectors. Pol: polarizer; λ/2: half-wave plate; OBJ: objective; PMT; photomultiplier tubes. A sample Stokes continuum spectrum entering the microscope is provided in the inset.

Fig. 2
Fig. 2

Potato starch grains. (a) Overlaid CARS (red) and SHG (green) images of potato starch grains in which striations associated with alternating crystalline and amorphous layers are clearly visible and appear to be anti-correlated between SHG and CARS. The pump and Stokes beams are polarized in the vertical direction. The 512 × 512 pixel image represents a Kalman average of 5 scans, acquired in a total of 5 seconds. (b) Nonresonant-background normalized CARS spectrum of starch sampled from the region of interest outlined in yellow in (a), and shown together with a representative spectrum for DMSO for comparison. (c) Start, middle, and end frames from a movie of a potato starch grain swelling upon heating in excess water (Media 1). Elapsed time between the first and last frames is approximately 150 seconds.

Fig. 3
Fig. 3

Rice starch grain swelling. (a) Start, middle, and end frames from a movie of a rice starch grain swelling upon heating in excess water (Media 2). CARS and SHG images are shown side-by-side on the left and right, respectively. The color-scheme for SHG is chosen to emphasize contrast (blue-to-red-to-white; low-to-high). Disappearance of SHG signal is seen long before disappearance of the CARS signal, strongly suggesting that crystallinity is reduced before the bulk dilution of starch (swelling) takes place. Elapsed time between the first and last frames is approximately 150 seconds. (b) CARS spectra taken before the onset of swelling (from ROI 1 in (a)) and after swelling (from ROI 2 and 3 in (a)), indicating that the swollen grain is intact and still surrounded by a diluted starch layer. The spectra in ROI 1, 2, and 3 are normalized to the spectra from the surrounding water (not shown).

Fig. 4
Fig. 4

CARS and SHG from a cotton fiber in water. (a) The CARS signal (red) illuminates the fiber more uniformly than does the striped SHG signal (cyan). The Stokes and pump beams are aligned vertically with respect to the image. (b) Representative CARS spectra of cellulose and background water are taken from the ROIs in (a). The O-H stretch region in cotton cellulose is clearly distinct from the broad and mostly featureless O-H region in water.

Fig. 5
Fig. 5

CARS and SHG from a cotton fiber in deuterated water. (a) A CARS image taken at 2900 cm−1. The Stokes and pump beams are aligned vertically with respect to the image. (b) Simultaneously-obtained SHG image. (c) CARS spectra from the two ROI indicated in (a), showing clear differences in the relative signal intensities at the C-H and O-H stretch regions. (d) An overlay map of the ratio of the pixel-by-pixel CARS signals at 2900/2960 cm−1 (red) and 2900/3220 cm−1 (green). The color maps scale such that an average ratio of 1 is background and a ratio of 4.3 is maximum intensity in the green channel and a ratio of 12.6 is maximum in the red channel. The average value in the red channel over ROI 1 is 4.5.

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