Abstract

Previously unobtainable measurements of alveolar pH were obtained using an endoscope-deployable optrode. The pH sensing was achieved using functionalized gold nanoshell sensors and surface enhanced Raman spectroscopy (SERS). The optrode consisted of an asymmetric dual-core optical fiber designed for spatially separating the optical pump delivery and signal collection, in order to circumvent the unwanted Raman signal generated within the fiber. Using this approach, we demonstrate a ~100-fold increase in SERS signal-to-fiber background ratio, and demonstrate multiple site pH sensing with a measurement accuracy of ± 0.07 pH units in the respiratory acini of an ex vivo ovine lung model. We also demonstrate that alveolar pH changes in response to ventilation.

© 2016 Optical Society of America

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References

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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  40. S. A. Grant and R. S. Glass, “Sol-gel-based biosensor for use in stroke treatment,” IEEE Trans. Biomed. Eng. 46(10), 1207–1211 (1999).
    [Crossref] [PubMed]

2016 (1)

J. Koivisto, X. Chen, S. Donnini, T. Lahtinen, H. Häkkinen, G. Groenhof, and M. Pettersson, “Acid–Base Properties and Surface Charge Distribution of the Water-Soluble Au102(pMBA)44 Nanocluster,” J. Phys. Chem. C 120(18), 10041–10050 (2016).
[Crossref]

2015 (3)

A. Jaworska, L. E. Jamieson, K. Malek, C. J. Campbell, J. Choo, S. Chlopicki, and M. Baranska, “SERS-based monitoring of the intracellular pH in endothelial cells: the influence of the extracellular environment and tumour necrosis factor-α,” Analyst (Lond.) 140(7), 2321–2329 (2015).
[Crossref] [PubMed]

E. Garai, S. Sensarn, C. L. Zavaleta, N. O. Loewke, S. Rogalla, M. J. Mandella, S. A. Felt, S. Friedland, J. T. C. Liu, S. S. Gambhir, and C. H. Contag, “A Real-Time Clinical Endoscopic System for Intraluminal, Multiplexed Imaging of Surface-Enhanced Raman Scattering Nanoparticles,” PLoS One 10(4), e0123185 (2015).
[Crossref] [PubMed]

A. Ricciardi, A. Crescitelli, P. Vaiano, G. Quero, M. Consales, M. Pisco, E. Esposito, and A. Cusano, “Lab-on-fiber technology: a new vision for chemical and biological sensing,” Analyst (Lond.) 140(24), 8068–8079 (2015).
[Crossref] [PubMed]

2014 (2)

D. Choudhury, J. R. Macdonald, and A. K. Kar, “Ultrafast laser inscription: perspectives on future integrated applications,” Laser Photonics Rev. 8(6), 827–846 (2014).
[Crossref]

Y. W. Wang, A. Khan, S. Y. Leigh, D. Wang, Y. Chen, D. Meza, and J. T. C. Liu, “Comprehensive spectral endoscopy of topically applied SERS nanoparticles in the rat esophagus,” Biomed. Opt. Express 5(9), 2883–2895 (2014).
[Crossref] [PubMed]

2013 (5)

J. S. Hartley, S. Juodkazis, and P. R. Stoddart, “Optical fibers for miniaturized surface-enhanced Raman-scattering probes,” Appl. Opt. 52(34), 8388–8393 (2013).
[Crossref] [PubMed]

D. I. Ellis, D. P. Cowcher, L. Ashton, S. O’Hagan, and R. Goodacre, “Illuminating disease and enlightening biomedicine: Raman spectroscopy as a diagnostic tool,” Analyst (Lond.) 138(14), 3871–3884 (2013).
[Crossref] [PubMed]

B. B. Praveen, C. Steuwe, M. Mazilu, K. Dholakia, and S. Mahajan, “Wavelength modulated surface enhanced (resonance) Raman scattering for background-free detection,” Analyst (Lond.) 138(10), 2816–2820 (2013).
[Crossref] [PubMed]

Y. Liu, H. Yuan, A. M. Fales, and T. Vo-Dinh, “pH-sensing nanostar probe using surface-enhanced Raman scattering (SERS): theoretical and experimental studies,” J. Raman Spectrosc. 44(7), 980–986 (2013).
[Crossref]

W. F. Walkenhorst, J. W. Klein, P. Vo, and W. C. Wimley, “pH Dependence of Microbe Sterilization by Cationic Antimicrobial Peptides,” Antimicrob. Agents Chemother. 57(7), 3312–3320 (2013).
[Crossref] [PubMed]

2012 (3)

A. A. Pezzulo, X. X. Tang, M. J. Hoegger, M. H. Abou Alaiwa, S. Ramachandran, T. O. Moninger, P. H. Karp, C. L. Wohlford-Lenane, H. P. Haagsman, M. van Eijk, B. Bánfi, A. R. Horswill, D. A. Stoltz, P. B. McCray, M. J. Welsh, and J. Zabner, “Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung,” Nature 487(7405), 109–113 (2012).
[Crossref] [PubMed]

F. Wang, R. G. Widejko, Z. Yang, K. T. Nguyen, H. Chen, L. P. Fernando, K. A. Christensen, and J. N. Anker, “Surface-Enhanced Raman Scattering Detection of pH with Silica-Encapsulated 4-Mercaptobenzoic Acid-Functionalized Silver Nanoparticles,” Anal. Chem. 84(18), 8013–8019 (2012).
[Crossref] [PubMed]

S. Dochow, I. Latka, M. Becker, R. Spittel, J. Kobelke, K. Schuster, A. Graf, S. Brückner, S. Unger, M. Rothhardt, B. Dietzek, C. Krafft, and J. Popp, “Multicore fiber with integrated fiber Bragg gratings for background-free Raman sensing,” Opt. Express 20(18), 20156–20169 (2012).
[Crossref] [PubMed]

2011 (1)

X. Yang, C. Shi, R. Newhouse, J. Z. Zhang, and C. Gu, “Hollow-Core Photonic Crystal Fibers for Surface-Enhanced Raman Scattering Probes,” Int. J. Opt. 2011, 1–11 (2011).
[Crossref]

2010 (1)

G. F. S. Andrade, M. Fan, and A. G. Brolo, “Multilayer silver nanoparticles-modified optical fiber tip for high performance SERS remote sensing,” Biosens. Bioelectron. 25(10), 2270–2275 (2010).
[Crossref] [PubMed]

2009 (2)

P. R. Stoddart and D. J. White, “Optical fibre SERS sensors,” Anal. Bioanal. Chem. 394(7), 1761–1774 (2009).
[Crossref] [PubMed]

E. J. Smythe, M. D. Dickey, J. Bao, G. M. Whitesides, and F. Capasso, “Optical Antenna Arrays on a fiber Facet for in Situ Surface-Enhanced Raman Scattering Detection,” Nano Lett. 9(3), 1132–1138 (2009).
[Crossref] [PubMed]

2008 (1)

P. L. Stiles, J. A. Dieringer, N. C. Shah, and R. P. Van Duyne, “Surface-Enhanced Raman Spectroscopy,” Annu. Rev. Anal. Chem. (Palo Alto, Calif.) 1(1), 601–626 (2008).
[Crossref] [PubMed]

2006 (3)

S. W. Bishnoi, C. J. Rozell, C. S. Levin, M. K. Gheith, B. R. Johnson, D. H. Johnson, and N. J. Halas, “All-Optical Nanoscale pH meter,” Nano Lett. 6(8), 1687–1692 (2006).
[Crossref] [PubMed]

H. Yan, C. Gu, C. Yang, J. Liu, G. Jin, J. Zhang, L. Hou, and Y. Yao, “Hollow core photonic crystal fiber surface-enhanced Raman probe,” Appl. Phys. Lett. 89(20), 204101 (2006).
[Crossref]

D. Pristinski and H. Du, “Solid-core photonic crystal fiber as a Raman spectroscopy platform with a silica core as an internal reference,” Opt. Lett. 31(22), 3246–3248 (2006).
[Crossref] [PubMed]

2005 (4)

G. Schulze, A. Jirasek, M. M. L. Yu, A. Lim, R. F. B. Turner, and M. W. Blades, “Investigation of selected baseline removal techniques as candidates for automated implementation,” Appl. Spectrosc. 59(5), 545–574 (2005).
[Crossref] [PubMed]

Y. Komachi, H. Sato, K. Aizawa, and H. Tashiro, “Micro-optical fiber probe for use in an intravascular Raman endoscope,” Appl. Opt. 44(22), 4722–4732 (2005).
[Crossref] [PubMed]

J. T. Motz, S. J. Gandhi, O. R. Scepanovic, A. S. Haka, J. R. Kramer, R. R. Dasari, and M. S. Feld, “Real-time Raman system for in vivo disease diagnosis,” J. Biomed. Opt. 10(3), 031113 (2005).
[Crossref] [PubMed]

A. Dalhoff, S. Schubert, and U. Ullmann, “Effect of pH on the in Vitro Activity of and Propensity for Emergence of Resistance to Fluoroquinolones, Macrolides, and a Ketolide,” Infection 33(S2Suppl 2), 36–43 (2005).
[Crossref] [PubMed]

2004 (2)

2003 (2)

E. M. Scarpelli, “Physiology of the Alveolar Surface Network,” Comp. Biochem. Physiol. A Mol. Integr. Physiol. 135(1), 39–104 (2003).
[Crossref] [PubMed]

J. C. Knight, “Photonic crystal fibres,” Nature 424(6950), 847–851 (2003).
[Crossref] [PubMed]

2001 (2)

A. Marcinkevičius, S. Juodkazis, M. Watanabe, M. Miwa, S. Matsuo, H. Misawa, and J. Nishii, “Femtosecond laser-assisted three-dimensional microfabrication in silica,” Opt. Lett. 26(5), 277–279 (2001).
[Crossref] [PubMed]

S. Jayaraman, Y. Song, and A. S. Verkman, “Airway surface liquid pH in well-differentiated airway epithelial cell cultures and mouse trachea,” Am. J. Physiol. Cell Physiol. 281(5), C1504–C1511 (2001).
[PubMed]

2000 (1)

A. Bidani, B. S. Reisner, A. K. Haque, J. Wen, R. E. Helmer, D. M. Tuazon, and T. A. Heming, “Bactericidal Activity Of Alveolar Macrophages is Suppressed by V-ATPase Inhibition,” Lung 178(2), 91–104 (2000).
[Crossref] [PubMed]

1999 (2)

A. S. Trevani, G. Andonegui, M. Giordano, D. H. López, R. Gamberale, F. Minucci, and J. R. Geffner, “Extracellular Acidification Induces Human Neutrophil Activation,” J. Immunol. 162(8), 4849–4857 (1999).
[PubMed]

S. A. Grant and R. S. Glass, “Sol-gel-based biosensor for use in stroke treatment,” IEEE Trans. Biomed. Eng. 46(10), 1207–1211 (1999).
[Crossref] [PubMed]

1995 (1)

A. Bidani and T. A. Heming, “Effects of bafilomycin A1 on functional capabilities of LPS-activated alveolar macrophages,” J. Leukoc. Biol. 57(2), 275–281 (1995).
[PubMed]

1983 (1)

C. R. Bodem, L. M. Lampton, D. P. Miller, E. F. Tarka, and E. D. Everett, “Endobronchial pH. Relevance of aminoglycoside activity in gram-negative bacillary pneumonia,” Am. Rev. Respir. Dis. 127(1), 39–41 (1983).
[Crossref] [PubMed]

1981 (1)

D. W. Nielson, J. Goerke, and J. A. Clements, “Alveolar subphase pH in the lungs of anesthetized rabbits,” Proc. Natl. Acad. Sci. U.S.A. 78(11), 7119–7123 (1981).
[Crossref] [PubMed]

Abou Alaiwa, M. H.

A. A. Pezzulo, X. X. Tang, M. J. Hoegger, M. H. Abou Alaiwa, S. Ramachandran, T. O. Moninger, P. H. Karp, C. L. Wohlford-Lenane, H. P. Haagsman, M. van Eijk, B. Bánfi, A. R. Horswill, D. A. Stoltz, P. B. McCray, M. J. Welsh, and J. Zabner, “Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung,” Nature 487(7405), 109–113 (2012).
[Crossref] [PubMed]

Aizawa, K.

Andonegui, G.

A. S. Trevani, G. Andonegui, M. Giordano, D. H. López, R. Gamberale, F. Minucci, and J. R. Geffner, “Extracellular Acidification Induces Human Neutrophil Activation,” J. Immunol. 162(8), 4849–4857 (1999).
[PubMed]

Andrade, G. F. S.

G. F. S. Andrade, M. Fan, and A. G. Brolo, “Multilayer silver nanoparticles-modified optical fiber tip for high performance SERS remote sensing,” Biosens. Bioelectron. 25(10), 2270–2275 (2010).
[Crossref] [PubMed]

Anker, J. N.

F. Wang, R. G. Widejko, Z. Yang, K. T. Nguyen, H. Chen, L. P. Fernando, K. A. Christensen, and J. N. Anker, “Surface-Enhanced Raman Scattering Detection of pH with Silica-Encapsulated 4-Mercaptobenzoic Acid-Functionalized Silver Nanoparticles,” Anal. Chem. 84(18), 8013–8019 (2012).
[Crossref] [PubMed]

Ashton, L.

D. I. Ellis, D. P. Cowcher, L. Ashton, S. O’Hagan, and R. Goodacre, “Illuminating disease and enlightening biomedicine: Raman spectroscopy as a diagnostic tool,” Analyst (Lond.) 138(14), 3871–3884 (2013).
[Crossref] [PubMed]

Bánfi, B.

A. A. Pezzulo, X. X. Tang, M. J. Hoegger, M. H. Abou Alaiwa, S. Ramachandran, T. O. Moninger, P. H. Karp, C. L. Wohlford-Lenane, H. P. Haagsman, M. van Eijk, B. Bánfi, A. R. Horswill, D. A. Stoltz, P. B. McCray, M. J. Welsh, and J. Zabner, “Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung,” Nature 487(7405), 109–113 (2012).
[Crossref] [PubMed]

Bao, J.

E. J. Smythe, M. D. Dickey, J. Bao, G. M. Whitesides, and F. Capasso, “Optical Antenna Arrays on a fiber Facet for in Situ Surface-Enhanced Raman Scattering Detection,” Nano Lett. 9(3), 1132–1138 (2009).
[Crossref] [PubMed]

Baranska, M.

A. Jaworska, L. E. Jamieson, K. Malek, C. J. Campbell, J. Choo, S. Chlopicki, and M. Baranska, “SERS-based monitoring of the intracellular pH in endothelial cells: the influence of the extracellular environment and tumour necrosis factor-α,” Analyst (Lond.) 140(7), 2321–2329 (2015).
[Crossref] [PubMed]

Becker, M.

Bidani, A.

A. W. Ng, A. Bidani, and T. A. Heming, “Innate Host Defense of the Lung: Effects of Lung-Lining Fluid pH,” Lung 182(5), 297–317 (2004).
[Crossref] [PubMed]

A. Bidani, B. S. Reisner, A. K. Haque, J. Wen, R. E. Helmer, D. M. Tuazon, and T. A. Heming, “Bactericidal Activity Of Alveolar Macrophages is Suppressed by V-ATPase Inhibition,” Lung 178(2), 91–104 (2000).
[Crossref] [PubMed]

A. Bidani and T. A. Heming, “Effects of bafilomycin A1 on functional capabilities of LPS-activated alveolar macrophages,” J. Leukoc. Biol. 57(2), 275–281 (1995).
[PubMed]

Bishnoi, S. W.

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Y. Liu, H. Yuan, A. M. Fales, and T. Vo-Dinh, “pH-sensing nanostar probe using surface-enhanced Raman scattering (SERS): theoretical and experimental studies,” J. Raman Spectrosc. 44(7), 980–986 (2013).
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E. Garai, S. Sensarn, C. L. Zavaleta, N. O. Loewke, S. Rogalla, M. J. Mandella, S. A. Felt, S. Friedland, J. T. C. Liu, S. S. Gambhir, and C. H. Contag, “A Real-Time Clinical Endoscopic System for Intraluminal, Multiplexed Imaging of Surface-Enhanced Raman Scattering Nanoparticles,” PLoS One 10(4), e0123185 (2015).
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A. S. Trevani, G. Andonegui, M. Giordano, D. H. López, R. Gamberale, F. Minucci, and J. R. Geffner, “Extracellular Acidification Induces Human Neutrophil Activation,” J. Immunol. 162(8), 4849–4857 (1999).
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Matsuo, S.

Mazilu, M.

B. B. Praveen, C. Steuwe, M. Mazilu, K. Dholakia, and S. Mahajan, “Wavelength modulated surface enhanced (resonance) Raman scattering for background-free detection,” Analyst (Lond.) 138(10), 2816–2820 (2013).
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A. A. Pezzulo, X. X. Tang, M. J. Hoegger, M. H. Abou Alaiwa, S. Ramachandran, T. O. Moninger, P. H. Karp, C. L. Wohlford-Lenane, H. P. Haagsman, M. van Eijk, B. Bánfi, A. R. Horswill, D. A. Stoltz, P. B. McCray, M. J. Welsh, and J. Zabner, “Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung,” Nature 487(7405), 109–113 (2012).
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Meza, D.

Miller, D. P.

C. R. Bodem, L. M. Lampton, D. P. Miller, E. F. Tarka, and E. D. Everett, “Endobronchial pH. Relevance of aminoglycoside activity in gram-negative bacillary pneumonia,” Am. Rev. Respir. Dis. 127(1), 39–41 (1983).
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A. S. Trevani, G. Andonegui, M. Giordano, D. H. López, R. Gamberale, F. Minucci, and J. R. Geffner, “Extracellular Acidification Induces Human Neutrophil Activation,” J. Immunol. 162(8), 4849–4857 (1999).
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J. T. Motz, S. J. Gandhi, O. R. Scepanovic, A. S. Haka, J. R. Kramer, R. R. Dasari, and M. S. Feld, “Real-time Raman system for in vivo disease diagnosis,” J. Biomed. Opt. 10(3), 031113 (2005).
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Praveen, B. B.

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A. A. Pezzulo, X. X. Tang, M. J. Hoegger, M. H. Abou Alaiwa, S. Ramachandran, T. O. Moninger, P. H. Karp, C. L. Wohlford-Lenane, H. P. Haagsman, M. van Eijk, B. Bánfi, A. R. Horswill, D. A. Stoltz, P. B. McCray, M. J. Welsh, and J. Zabner, “Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung,” Nature 487(7405), 109–113 (2012).
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J. T. Motz, S. J. Gandhi, O. R. Scepanovic, A. S. Haka, J. R. Kramer, R. R. Dasari, and M. S. Feld, “Real-time Raman system for in vivo disease diagnosis,” J. Biomed. Opt. 10(3), 031113 (2005).
[Crossref] [PubMed]

Schubert, S.

A. Dalhoff, S. Schubert, and U. Ullmann, “Effect of pH on the in Vitro Activity of and Propensity for Emergence of Resistance to Fluoroquinolones, Macrolides, and a Ketolide,” Infection 33(S2Suppl 2), 36–43 (2005).
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Schulze, G.

Schuster, K.

Sensarn, S.

E. Garai, S. Sensarn, C. L. Zavaleta, N. O. Loewke, S. Rogalla, M. J. Mandella, S. A. Felt, S. Friedland, J. T. C. Liu, S. S. Gambhir, and C. H. Contag, “A Real-Time Clinical Endoscopic System for Intraluminal, Multiplexed Imaging of Surface-Enhanced Raman Scattering Nanoparticles,” PLoS One 10(4), e0123185 (2015).
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Shah, N. C.

P. L. Stiles, J. A. Dieringer, N. C. Shah, and R. P. Van Duyne, “Surface-Enhanced Raman Spectroscopy,” Annu. Rev. Anal. Chem. (Palo Alto, Calif.) 1(1), 601–626 (2008).
[Crossref] [PubMed]

Shi, C.

X. Yang, C. Shi, R. Newhouse, J. Z. Zhang, and C. Gu, “Hollow-Core Photonic Crystal Fibers for Surface-Enhanced Raman Scattering Probes,” Int. J. Opt. 2011, 1–11 (2011).
[Crossref]

Smythe, E. J.

E. J. Smythe, M. D. Dickey, J. Bao, G. M. Whitesides, and F. Capasso, “Optical Antenna Arrays on a fiber Facet for in Situ Surface-Enhanced Raman Scattering Detection,” Nano Lett. 9(3), 1132–1138 (2009).
[Crossref] [PubMed]

Song, Y.

S. Jayaraman, Y. Song, and A. S. Verkman, “Airway surface liquid pH in well-differentiated airway epithelial cell cultures and mouse trachea,” Am. J. Physiol. Cell Physiol. 281(5), C1504–C1511 (2001).
[PubMed]

Spittel, R.

Steuwe, C.

B. B. Praveen, C. Steuwe, M. Mazilu, K. Dholakia, and S. Mahajan, “Wavelength modulated surface enhanced (resonance) Raman scattering for background-free detection,” Analyst (Lond.) 138(10), 2816–2820 (2013).
[Crossref] [PubMed]

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P. L. Stiles, J. A. Dieringer, N. C. Shah, and R. P. Van Duyne, “Surface-Enhanced Raman Spectroscopy,” Annu. Rev. Anal. Chem. (Palo Alto, Calif.) 1(1), 601–626 (2008).
[Crossref] [PubMed]

Stoddart, P. R.

Stoltz, D. A.

A. A. Pezzulo, X. X. Tang, M. J. Hoegger, M. H. Abou Alaiwa, S. Ramachandran, T. O. Moninger, P. H. Karp, C. L. Wohlford-Lenane, H. P. Haagsman, M. van Eijk, B. Bánfi, A. R. Horswill, D. A. Stoltz, P. B. McCray, M. J. Welsh, and J. Zabner, “Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung,” Nature 487(7405), 109–113 (2012).
[Crossref] [PubMed]

Tang, X. X.

A. A. Pezzulo, X. X. Tang, M. J. Hoegger, M. H. Abou Alaiwa, S. Ramachandran, T. O. Moninger, P. H. Karp, C. L. Wohlford-Lenane, H. P. Haagsman, M. van Eijk, B. Bánfi, A. R. Horswill, D. A. Stoltz, P. B. McCray, M. J. Welsh, and J. Zabner, “Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung,” Nature 487(7405), 109–113 (2012).
[Crossref] [PubMed]

Tarka, E. F.

C. R. Bodem, L. M. Lampton, D. P. Miller, E. F. Tarka, and E. D. Everett, “Endobronchial pH. Relevance of aminoglycoside activity in gram-negative bacillary pneumonia,” Am. Rev. Respir. Dis. 127(1), 39–41 (1983).
[Crossref] [PubMed]

Tashiro, H.

Trevani, A. S.

A. S. Trevani, G. Andonegui, M. Giordano, D. H. López, R. Gamberale, F. Minucci, and J. R. Geffner, “Extracellular Acidification Induces Human Neutrophil Activation,” J. Immunol. 162(8), 4849–4857 (1999).
[PubMed]

Tuazon, D. M.

A. Bidani, B. S. Reisner, A. K. Haque, J. Wen, R. E. Helmer, D. M. Tuazon, and T. A. Heming, “Bactericidal Activity Of Alveolar Macrophages is Suppressed by V-ATPase Inhibition,” Lung 178(2), 91–104 (2000).
[Crossref] [PubMed]

Turner, R. F. B.

Ullmann, U.

A. Dalhoff, S. Schubert, and U. Ullmann, “Effect of pH on the in Vitro Activity of and Propensity for Emergence of Resistance to Fluoroquinolones, Macrolides, and a Ketolide,” Infection 33(S2Suppl 2), 36–43 (2005).
[Crossref] [PubMed]

Unger, S.

Vaiano, P.

A. Ricciardi, A. Crescitelli, P. Vaiano, G. Quero, M. Consales, M. Pisco, E. Esposito, and A. Cusano, “Lab-on-fiber technology: a new vision for chemical and biological sensing,” Analyst (Lond.) 140(24), 8068–8079 (2015).
[Crossref] [PubMed]

Van Duyne, R. P.

P. L. Stiles, J. A. Dieringer, N. C. Shah, and R. P. Van Duyne, “Surface-Enhanced Raman Spectroscopy,” Annu. Rev. Anal. Chem. (Palo Alto, Calif.) 1(1), 601–626 (2008).
[Crossref] [PubMed]

van Eijk, M.

A. A. Pezzulo, X. X. Tang, M. J. Hoegger, M. H. Abou Alaiwa, S. Ramachandran, T. O. Moninger, P. H. Karp, C. L. Wohlford-Lenane, H. P. Haagsman, M. van Eijk, B. Bánfi, A. R. Horswill, D. A. Stoltz, P. B. McCray, M. J. Welsh, and J. Zabner, “Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung,” Nature 487(7405), 109–113 (2012).
[Crossref] [PubMed]

Verkman, A. S.

S. Jayaraman, Y. Song, and A. S. Verkman, “Airway surface liquid pH in well-differentiated airway epithelial cell cultures and mouse trachea,” Am. J. Physiol. Cell Physiol. 281(5), C1504–C1511 (2001).
[PubMed]

Vo, P.

W. F. Walkenhorst, J. W. Klein, P. Vo, and W. C. Wimley, “pH Dependence of Microbe Sterilization by Cationic Antimicrobial Peptides,” Antimicrob. Agents Chemother. 57(7), 3312–3320 (2013).
[Crossref] [PubMed]

Vo-Dinh, T.

Y. Liu, H. Yuan, A. M. Fales, and T. Vo-Dinh, “pH-sensing nanostar probe using surface-enhanced Raman scattering (SERS): theoretical and experimental studies,” J. Raman Spectrosc. 44(7), 980–986 (2013).
[Crossref]

Walkenhorst, W. F.

W. F. Walkenhorst, J. W. Klein, P. Vo, and W. C. Wimley, “pH Dependence of Microbe Sterilization by Cationic Antimicrobial Peptides,” Antimicrob. Agents Chemother. 57(7), 3312–3320 (2013).
[Crossref] [PubMed]

Wang, D.

Wang, F.

F. Wang, R. G. Widejko, Z. Yang, K. T. Nguyen, H. Chen, L. P. Fernando, K. A. Christensen, and J. N. Anker, “Surface-Enhanced Raman Scattering Detection of pH with Silica-Encapsulated 4-Mercaptobenzoic Acid-Functionalized Silver Nanoparticles,” Anal. Chem. 84(18), 8013–8019 (2012).
[Crossref] [PubMed]

Wang, Y. W.

Watanabe, M.

Welsh, M. J.

A. A. Pezzulo, X. X. Tang, M. J. Hoegger, M. H. Abou Alaiwa, S. Ramachandran, T. O. Moninger, P. H. Karp, C. L. Wohlford-Lenane, H. P. Haagsman, M. van Eijk, B. Bánfi, A. R. Horswill, D. A. Stoltz, P. B. McCray, M. J. Welsh, and J. Zabner, “Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung,” Nature 487(7405), 109–113 (2012).
[Crossref] [PubMed]

Wen, J.

A. Bidani, B. S. Reisner, A. K. Haque, J. Wen, R. E. Helmer, D. M. Tuazon, and T. A. Heming, “Bactericidal Activity Of Alveolar Macrophages is Suppressed by V-ATPase Inhibition,” Lung 178(2), 91–104 (2000).
[Crossref] [PubMed]

White, D. J.

P. R. Stoddart and D. J. White, “Optical fibre SERS sensors,” Anal. Bioanal. Chem. 394(7), 1761–1774 (2009).
[Crossref] [PubMed]

Whitesides, G. M.

E. J. Smythe, M. D. Dickey, J. Bao, G. M. Whitesides, and F. Capasso, “Optical Antenna Arrays on a fiber Facet for in Situ Surface-Enhanced Raman Scattering Detection,” Nano Lett. 9(3), 1132–1138 (2009).
[Crossref] [PubMed]

Widejko, R. G.

F. Wang, R. G. Widejko, Z. Yang, K. T. Nguyen, H. Chen, L. P. Fernando, K. A. Christensen, and J. N. Anker, “Surface-Enhanced Raman Scattering Detection of pH with Silica-Encapsulated 4-Mercaptobenzoic Acid-Functionalized Silver Nanoparticles,” Anal. Chem. 84(18), 8013–8019 (2012).
[Crossref] [PubMed]

Wimley, W. C.

W. F. Walkenhorst, J. W. Klein, P. Vo, and W. C. Wimley, “pH Dependence of Microbe Sterilization by Cationic Antimicrobial Peptides,” Antimicrob. Agents Chemother. 57(7), 3312–3320 (2013).
[Crossref] [PubMed]

Wohlford-Lenane, C. L.

A. A. Pezzulo, X. X. Tang, M. J. Hoegger, M. H. Abou Alaiwa, S. Ramachandran, T. O. Moninger, P. H. Karp, C. L. Wohlford-Lenane, H. P. Haagsman, M. van Eijk, B. Bánfi, A. R. Horswill, D. A. Stoltz, P. B. McCray, M. J. Welsh, and J. Zabner, “Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung,” Nature 487(7405), 109–113 (2012).
[Crossref] [PubMed]

Yan, H.

H. Yan, C. Gu, C. Yang, J. Liu, G. Jin, J. Zhang, L. Hou, and Y. Yao, “Hollow core photonic crystal fiber surface-enhanced Raman probe,” Appl. Phys. Lett. 89(20), 204101 (2006).
[Crossref]

Yang, C.

H. Yan, C. Gu, C. Yang, J. Liu, G. Jin, J. Zhang, L. Hou, and Y. Yao, “Hollow core photonic crystal fiber surface-enhanced Raman probe,” Appl. Phys. Lett. 89(20), 204101 (2006).
[Crossref]

Yang, X.

X. Yang, C. Shi, R. Newhouse, J. Z. Zhang, and C. Gu, “Hollow-Core Photonic Crystal Fibers for Surface-Enhanced Raman Scattering Probes,” Int. J. Opt. 2011, 1–11 (2011).
[Crossref]

Yang, Z.

F. Wang, R. G. Widejko, Z. Yang, K. T. Nguyen, H. Chen, L. P. Fernando, K. A. Christensen, and J. N. Anker, “Surface-Enhanced Raman Scattering Detection of pH with Silica-Encapsulated 4-Mercaptobenzoic Acid-Functionalized Silver Nanoparticles,” Anal. Chem. 84(18), 8013–8019 (2012).
[Crossref] [PubMed]

Yao, Y.

H. Yan, C. Gu, C. Yang, J. Liu, G. Jin, J. Zhang, L. Hou, and Y. Yao, “Hollow core photonic crystal fiber surface-enhanced Raman probe,” Appl. Phys. Lett. 89(20), 204101 (2006).
[Crossref]

Yu, M. M. L.

Yuan, H.

Y. Liu, H. Yuan, A. M. Fales, and T. Vo-Dinh, “pH-sensing nanostar probe using surface-enhanced Raman scattering (SERS): theoretical and experimental studies,” J. Raman Spectrosc. 44(7), 980–986 (2013).
[Crossref]

Zabner, J.

A. A. Pezzulo, X. X. Tang, M. J. Hoegger, M. H. Abou Alaiwa, S. Ramachandran, T. O. Moninger, P. H. Karp, C. L. Wohlford-Lenane, H. P. Haagsman, M. van Eijk, B. Bánfi, A. R. Horswill, D. A. Stoltz, P. B. McCray, M. J. Welsh, and J. Zabner, “Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung,” Nature 487(7405), 109–113 (2012).
[Crossref] [PubMed]

Zavaleta, C. L.

E. Garai, S. Sensarn, C. L. Zavaleta, N. O. Loewke, S. Rogalla, M. J. Mandella, S. A. Felt, S. Friedland, J. T. C. Liu, S. S. Gambhir, and C. H. Contag, “A Real-Time Clinical Endoscopic System for Intraluminal, Multiplexed Imaging of Surface-Enhanced Raman Scattering Nanoparticles,” PLoS One 10(4), e0123185 (2015).
[Crossref] [PubMed]

Zhang, J.

H. Yan, C. Gu, C. Yang, J. Liu, G. Jin, J. Zhang, L. Hou, and Y. Yao, “Hollow core photonic crystal fiber surface-enhanced Raman probe,” Appl. Phys. Lett. 89(20), 204101 (2006).
[Crossref]

Zhang, J. Z.

X. Yang, C. Shi, R. Newhouse, J. Z. Zhang, and C. Gu, “Hollow-Core Photonic Crystal Fibers for Surface-Enhanced Raman Scattering Probes,” Int. J. Opt. 2011, 1–11 (2011).
[Crossref]

Am. J. Physiol. Cell Physiol. (1)

S. Jayaraman, Y. Song, and A. S. Verkman, “Airway surface liquid pH in well-differentiated airway epithelial cell cultures and mouse trachea,” Am. J. Physiol. Cell Physiol. 281(5), C1504–C1511 (2001).
[PubMed]

Am. Rev. Respir. Dis. (1)

C. R. Bodem, L. M. Lampton, D. P. Miller, E. F. Tarka, and E. D. Everett, “Endobronchial pH. Relevance of aminoglycoside activity in gram-negative bacillary pneumonia,” Am. Rev. Respir. Dis. 127(1), 39–41 (1983).
[Crossref] [PubMed]

Anal. Bioanal. Chem. (1)

P. R. Stoddart and D. J. White, “Optical fibre SERS sensors,” Anal. Bioanal. Chem. 394(7), 1761–1774 (2009).
[Crossref] [PubMed]

Anal. Chem. (1)

F. Wang, R. G. Widejko, Z. Yang, K. T. Nguyen, H. Chen, L. P. Fernando, K. A. Christensen, and J. N. Anker, “Surface-Enhanced Raman Scattering Detection of pH with Silica-Encapsulated 4-Mercaptobenzoic Acid-Functionalized Silver Nanoparticles,” Anal. Chem. 84(18), 8013–8019 (2012).
[Crossref] [PubMed]

Analyst (Lond.) (4)

D. I. Ellis, D. P. Cowcher, L. Ashton, S. O’Hagan, and R. Goodacre, “Illuminating disease and enlightening biomedicine: Raman spectroscopy as a diagnostic tool,” Analyst (Lond.) 138(14), 3871–3884 (2013).
[Crossref] [PubMed]

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Annu. Rev. Anal. Chem. (Palo Alto, Calif.) (1)

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W. F. Walkenhorst, J. W. Klein, P. Vo, and W. C. Wimley, “pH Dependence of Microbe Sterilization by Cationic Antimicrobial Peptides,” Antimicrob. Agents Chemother. 57(7), 3312–3320 (2013).
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H. Yan, C. Gu, C. Yang, J. Liu, G. Jin, J. Zhang, L. Hou, and Y. Yao, “Hollow core photonic crystal fiber surface-enhanced Raman probe,” Appl. Phys. Lett. 89(20), 204101 (2006).
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E. M. Scarpelli, “Physiology of the Alveolar Surface Network,” Comp. Biochem. Physiol. A Mol. Integr. Physiol. 135(1), 39–104 (2003).
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A. S. Trevani, G. Andonegui, M. Giordano, D. H. López, R. Gamberale, F. Minucci, and J. R. Geffner, “Extracellular Acidification Induces Human Neutrophil Activation,” J. Immunol. 162(8), 4849–4857 (1999).
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Figures (8)

Fig. 1
Fig. 1 Schematic illustration of the fiber-optic sensing system and the miniaturized optrode for measuring alveolar pH. The packaged miniaturized optrode consisted of a 3 m long custom fabricated asymmetric dual-core optical fiber (outer diameter: 125 μm) and a bespoke distal end cap (outer diameter: 1.2 mm), assembled within a biocompatible tube (PEEK, outer diameter 1.5 mm). The fiber consists of a 2 μm diameter graded-index pump core (single mode at 785 nm) and a 28 μm diameter graded-index collection core that is multi-mode at the pump and signal wavelengths. The optrode was constructed by fusion splicing a short (~1 mm) section of a commercial multi-mode fiber (core diameter 50 μm, outer diameter 125 μm) onto the dual-core fiber. The end-face of the optrode was deposited with Au nanoshells functionalized with p-MBA as the pH sensing reporter molecule. The fiber-optic optrode was navigated through the working channel of a standard bronchoscope into the alveolar space of an ex vivo ovine lung model. A proximal end optical instrument (see Fig. 2) was built to collect and direct the SERS spectra encoding the pH information to a spectrometer. Post-acquisition, the data was processed using machine-learning algorithms to predict the unknown pH in the distal lung. Inset photograph: The packaged optrode emerging from the accessory channel of a bronchoscope. 4 distal end-caps are also shown alongside a one-penny coin.
Fig. 2
Fig. 2 A proximal-end optical instrument was used to input couple the excitation light into the SM core of the dual-core fiber and output couple the Raman-shifted signal light to the spectrometer. A continuous-wave 785 nm laser source (Thorlabs) with linewidth <0.1 nm was used as the pump source for this experiment. The 785 nm mode from a SM fiber (Thorlabs, 780-HP) was imaged at unit magnification using aspheric lenses (L1 & L2) onto the SM excitation core at the proximal end of the dual-core fiber. The SERS signal light from the MM core of the optrode was collected using lens L2 and, after passing through a long pass dichroic (DM), was imaged with unit magnification using the lens L3 and a fold mirror (FM 2) onto the step-index 50 μm core of a MM patch-cable which was attached to a spectrometer (Ocean Optics, QE Pro - 50 μm slit). In this background-suppressed mode, light in the SM core is explicitly excluded from being collected and routed to the spectrometer. Adjustment of fiber alignment allowed the instrument to be switched between background suppressed, and a more conventional non-suppressed mode, in which the same multi-mode core could be used for both excitation and collection. A short-pass filter (SP) was placed in the pump path before the dichroic to prevent the SERS signal being contaminated by long wavelength amplified spontaneous emission from the laser source. A long-pass filter (LP) was placed in the signal path to prevent 785 nm light from being coupled into the spectrometer. The spectral resolution was limited by the spectrometer to ~0.4 nm, narrower than the observed SERS spectral features (see Fig. 3(c)).
Fig. 3
Fig. 3 Background suppressed p-MBA SERS spectrum and its characteristics with respect to change in pH, observed using the packaged fiber-optic optrode. (a) p-MBA SERS spectrum acquired between 800 cm−1 and 2000 cm−1 when the MM core was used for both excitation and collection (normal mode). (b) p-MBA SERS spectrum acquired between 800 cm−1 and 2000 cm−1 when the SM and MM cores were used for excitation and collection respectively (background suppressed mode). Suppression of the fiber Raman background by ~100-fold was achieved in comparison to the spectrum shown in (a). (c) Characteristic p-MBA SERS spectrum acquired using the fiber-optic optrode. (d) p-MBA SERS spectrum from 1300 cm−1 to 1800 cm−1 showing pH sensitive response in the vicinity of 1380 cm−1 and 1700 cm−1. (e) Variation of the area under the curve (AUC) ratio with respect to pH in the range 4.0 – 9.0 obtained after computational data processing (see Section 3.1.1). The error bars represent the standard error of the mean over five technical replicate measurements, acquired over measurement intervals up to 9 hours. The extended time intervals between replicate measurements increase the extent of error bars. The intrinsic accuracy of the SERS measurements is analyzed separately (see Section 3.1.3).
Fig. 4
Fig. 4 Variation of area under the curve (AUC) ratio as a function of pH within the pH 6.0 – 7.0 range. The error bars represent the standard error of the mean over five technical replicate measurements, acquired over measurement intervals up to 4 hours.
Fig. 5
Fig. 5 Typical shape of p-MBA SERS, background and residual spectra acquired using the fiber optic optrode. The residual spectra were obtained using (a) a measured background spectrum and (b) background estimated using adaptive iterative reweighed penalized least squares, (airPLS). The measured background is subtracted by estimating its strength using airPLS by keeping the background (b) fixed and learning the coefficient ( c b i ) . We observe that although the measured background exhibits a lower envelope of a typical p-MBA SERS spectrum (obtained through the fiber) at Raman shifts lower than 1200 cm−1, it is not so at shifts higher than 1200 cm−1.
Fig. 6
Fig. 6 The area under the curve (AUC) ratio obtained at pH 6.4 and 7.4 plotted against time over 50 consecutive replicate measurements (a) with background suppression (b) without background suppression. The numbers in the insets represent the mean and standard deviation of the data for each pH respectively.
Fig. 7
Fig. 7 Alveolar space pH measured using the fiber-optic optrode in an ex vivo ovine lung model. (a) Photograph of the ex vivo ovine lung perfusion and ventilation set-up used for the experiment. a1: Incubator a2: Physiology monitor a3: Bronchoscopy screen a4: Ventilator and closed breathing circuit a5: Ventilated ovine lung a6: Water bath and perfusate circuit a7: Roller pump. (b) Photograph of the ex vivo ovine lung with numbers representing the six subsegments interrogated using the fiber-optic probe (c) Illustration showing the perfusion and ventilation circuits used in the experiment. 1: Ventilator, 2: Breathing circuit, 3: Incubator and humidifier, 4: Left atrial cannula, 5: Pulmonary artery cannula, 6: Roller pump, 7: Reservoir (d) p-MBA spectrum between 1300 cm−1 and 1800 cm−1, obtained from the sequential interrogation of the six distal subsegments shown in (b). (e) The alveolar pH measured using the fiber-optic optrode for the six subsegments (y-axis). The x-axis represents the pH measured using the commercial pH monitor at the incised locations for each subsegment. The numbers indicate the order in which the instilled subsegments were interrogated using the fiber-optic optrode. (f) Alveolar pH variation as a function of time in an ex vivo ovine lung model with ceased ventilation (t = 0) measured using the fiber-optic optrode. The variation of perfusate pH with time measured using a commercial pH probe is also shown.
Fig. 8
Fig. 8 Fabrication stages of the dual core fiber. Stage one, the formation of the stack to include the small excitation core. Pure silica rods (shown in grey) are stacked between two nested pure silica tubes, except that one of the rods contains a Ge-doped core (shown in blue) to form the small excitation core in the final fiber. Stage two, formation of the large collection core. A large rod with a Ge-doped core was inserted into the hollow preform drawn from the stack, then drawn down to form the final fiber. An optical micrograph of a transverse cross-section of the fiber is shown in the bottom right corner. The high-index core regions appear lighter in the image, with the small excitation core visible at “11 o'clock”. The scale bar is 20 µm.

Equations (3)

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s ˜ (pH,r)= c s r s(pH)+ c b r
( s ˜ b) T W( s ˜ b)+λ|| Δ 2 b| | 2
i ( s ˜ i c b i b) T W i ( s ˜ i c b i b)+λ|| Δ 2 b| | 2

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