Abstract

The intestinal mucosal barrier prevents macromolecules and pathogens from entering the circulatory stream. Tight junctions in this barrier are compromised in inflammatory bowel diseases, environmental enteropathy, and enteric dysfunction. Dual sugar absorption tests are a standard method for measuring gastrointestinal integrity, however, these are not clinically amenable. Herein, we report on a dual fluorophore system and fluorescence detection instrumentation for which gastrointestinal permeability is determined in a rat small bowel disease model from the longitudinal measured transdermal fluorescence of each fluorophore. This fluorophore technology enables a specimen-free, noninvasive, point-of-care gastrointestinal permeability measurement which should be translatable to human clinical studies.

Published by The Optical Society under the terms of the Creative Commons Attribution 4.0 License. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

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References

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  1. A. Michielan and R. D’Inca, “Intestinal Permeability in Inflammatory Bowel Disease: Pathogenesis, Clinical Evaluation, and Therapy of Leaky Gut,” Mediators Inflammation 2015, 1–10 (2015).
    [Crossref]
  2. E. Smecuol, J. C. Bai, H. Vazquez, Z. Kogan, A. Cabanne, S. Niveloni, S. Pedreira, L. Boerr, E. Mauriño, and J. B. Meddings, “Gastrointestinal permeability in celiac disease,” Gastroenterology 112(4), 1129–1136 (1997).
    [Crossref]
  3. J. E. Johansson and T. Ekman, “Gut toxicity during hemopoietic stem cell transplantation may predict acute graft-versus-host disease severity in patients,” Dig. Dis. Sci. 52(9), 2340–2345 (2007).
    [Crossref]
  4. A. Nier, A. J. Engstler, I. B. Maier, and I. Bergheim, “Markers of intestinal permeability are already altered in early stages of non-alcoholic fatty liver disease: Studies in children,” PLoS One 12(9), e0183282 (2017).
    [Crossref]
  5. L. Fotis, N. Shaikh, K. W. Baszis, C. M. Samson, R. Lev-Tzion, A. R. French, and P. I. Tarr, “Serologic Evidence of Gut-driven Systemic Inflammation in Juvenile Idiopathic Arthritis,” J. Rheumatol. 44(11), 1624–1631 (2017)..
    [Crossref]
  6. C. W. Teshima, K. J. Goodman, M. El-Kalla, S. Turk, W. El-Matary, R. Valcheva, R. Danchak, M. Gordon, P. Ho, A. Mullins, D. Wong, D. Kao, J. Meddings, H. Huynh, and L. A. Dieleman, “Increased Intestinal Permeability in Relatives of Patients With Crohn's Disease Is Not Associated With Small Bowel Ulcerations,” Clin. Gastroenterol. Hepatol. 15(9), 1413–1418.e1 (2017)..
    [Crossref]
  7. S. Buhner, C. Buning, J. Genschel, K. Kling, D. Herrmann, A. Dignass, I. Kuechler, S. Krueger, H. H Schmidt, and H. Lochs, “Genetic basis for increased intestinal permeability in families with Crohn's disease: role of CARD15 3020insC mutation,” Gut 55(3), 342–347 (2006).
    [Crossref]
  8. M. Peeters, B. Geypens, D. Claus, H. Nevens, Y. Ghoos, G. Verbeke, F. Baert, S. Vermeire, R. Vlietinck, and P. Rutgeerts, “Clustering of increased small intestinal permeability in families with Crohn's disease,” Gastroenterology 113(3), 802–807 (1997).
    [Crossref]
  9. M. D. Kappelman, K. R. Moore, and J. K. Allen, “Recent Trends in the Prevalence of Crohn’s Disease and Ulcerative Colitis in a Commercially Insured US Population,” Dig. Dis. Sci. 58(2), 519–525 (2013).
    [Crossref]
  10. D. T. Rubin, R. Mody, K. L. Davis, and C. C. Wang, “Real-world assessment of therapy changes, suboptimal treatment and associated costs in patients with ulcerative colitis or Crohn's disease,” Aliment. Pharmacol. Ther. 39(10), 1143–1155 (2014).
    [Crossref]
  11. S. Shah, M. Akbari, R. Vanga, C. P. Kelly, J. Hansen, T. Theethira, S. Tariq, M. Dennis, and D. A. Leffler, “Patient perception of treatment burden is high in celiac disease compared with other common conditions,” Am. J. Gastroenterol. 109(9), 1304–1311 (2014).
    [Crossref]
  12. B. G. Levesque, W. J. Sandborn, J. Ruel, B. G. Feagan, B. E. Sands, and J. F. Colombel, “Converging goals of treatment of inflammatory bowel disease from clinical trials and practice,” Gastroenterology 148(1), 37–51.e1 (2015).
    [Crossref]
  13. D. M. Denno, K. VanBuskirk, Z. C. Nelson, C. A. Musser, D. C. Hay Burgess, and P. Tarr, “Use of the lactulose to mannitol ratio to evaluate childhood environmental enteric dysfunction: a systematic review,” Clin. Infect. Dis. 59(suppl_4), S213–S219 (2014).
    [Crossref]
  14. I. R. Sequeira, R. G. Lentle, M. C. Kruger, and R. D. Hurst, “Standardising the lactulose mannitol test of gut permeability to minimise error and promote comparability,” PLoS One 9(6), e99256 (2014).
    [Crossref]
  15. A. M. Lostia, L. Lionetto, L. Principessa, M. Evangelisti, A. Gamba, M. P. Villa, and M. Simmaco, “A liquid chromatography/mass spectrometry method for the evaluation of intestinal permeability,” Clin. Biochem. 41(10-11), 887–892 (2008).
    [Crossref]
  16. G. O. Lee, P. Kosek, A. A. M. Lima, R. Singh, P. P. Yori, M. P. Olortegui, J. L. Lamsam, D. B. Oliveira, R. L. Guerrant, and M. Kosek, “Lactulose: mannitol diagnostic test by HPLC and LC-MSMS platforms: considerations for field studies of intestinal barrier function and environmental enteropathy,” J. Pediatr. Gastroenterol. Nutr. 59(4), 544–550 (2014).
    [Crossref]
  17. M. Camilleri, “Leaky gut: mechanisms, measurement and clinical implications in humans,” Gut 68(8), 1516–1526 (2019).
    [Crossref]
  18. R. B. Dorshow, C. Hall-Moore, N. Shaikh, M. R. Talcott, W. A. Faubion, T. E. Rogers, J. J. Shieh, M. P. Debreczeny, J. R. Johnson, R. B. Dyer, R. J. Singh, and P. I. Tarr, “Measurement of gut permeability using fluorescent tracer agent technology,” Sci. Rep. 7(1), 10888 (2017).
    [Crossref]
  19. K. Shiraia, A. Yanagisawab, H. Takahashib, K. Fukunishia, and M. Matsuokac, “Syntheses and fluorescent properties of 2,5-diamino-3,6-dicyanopyrazine dyes,” Dyes Pigm. 39(1), 49–68 (1998).
    [Crossref]
  20. R. Rajagopalan, W. L. Neumann, A. R. Poreddy, R. M. Fitch, J. N. Freskos, B. Asmelash, K. R. Gaston, K. P. Galen, J. J. Shieh, and R. M. Dorshow, “Hydrophilic pyrazine dyes as exogenous fluorescent tracer agents for real-time point-of-care measurement of glomerular filtration rate,” J. Med. Chem. 54(14), 5048–5058 (2011).
    [Crossref]
  21. N. M. Davies, M. R. Wright, and F. Jamali, “Antiinflammatory drug-induced small intestinal permeability: the rat is a suitable model,” Pharm. Res. 11(11), 1652–1656 (1994).
    [Crossref]
  22. C. Hesse, V. Razmovski-Naumovski, C. C. Duke, N. M. Davies, and B. D. Roufogalis, “Phytopreventative effects of Gynostemma pentaphyllum against acute Indomethacin-induced gastrointestinal and renal toxicity in rats,” Phytother. Res. 21(6), 523–530 (2007).
    [Crossref]
  23. M. Jacob, R. Foster, G. Sigthorsson, R. Simpson, and I. Bjarnason, “Role of bile in pathogenesis of indomethacin-induced enteropathy,” Arch. Toxicol. 81(4), 291–298 (2007)..
    [Crossref]
  24. H. Nishio, Y. Hayashi, S. Terashima, and K. Takeuchi, “Protective effect of pranlukast, a cysteinyl-leukotriene receptor 1 antagonist, on indomethacin-induced small intestinal damage in rats,” Inflammopharmacology 15(6), 266–272 (2007).
    [Crossref]
  25. Z. Sun, A. Lasson, K. Olanders, X. Deng, and R. Andersson, “Gut barrier permeability, reticuloendothelial system function and protease inhibitor levels following intestinal ischaemia and reperfusion–effects of pretreatment with N-acetyl-L-cysteine and indomethacin,” Dig. Liver Dis. 34(8), 560–569 (2002).
    [Crossref]
  26. H. Suzuki, N. Hanyou, I. Sonaka, and H. Minami, “An elemental diet controls inflammation in indomethacin-induced small bowel disease in rats: the role of low dietary fat and the elimination of dietary proteins,” Dig. Dis. Sci. 50(10), 1951–1958 (2005).
    [Crossref]
  27. M. R. Wright, N. M. Davies, and F. Jamali, “Toxicokinetics of indomethacin-induced intestinal permeability in the rat,” Pharmacol. Res. 35(6), 499–504 (1997).
    [Crossref]
  28. M. P. Debreczeny, R. Bates, R. M. Fitch, K. P. Galen, J. Ge, and R. B. Dorshow, “Human skin auto-fluorescence decay as a function of irradiance and skin type,” Proc. SPIE 7897, Optical Interactions with Tissue and Cells XXII, 78971T (2011).
  29. J. Schleusener, J. Lademann, and M. E. Darvin, “Depth-dependent autofluorescence photobleaching using 325, 473, 633, and 785 nm of porcine ear skin ex vivo,” J. Biomed. Opt. 22(9), 091503 (2017).
    [Crossref]
  30. R. S. Bradley and M. S. Thorniley, “A review of attenuation correction techniques for tissue fluorescence,” J. R. Soc., Interface 3(6), 1–13 (2006).
    [Crossref]

2019 (1)

M. Camilleri, “Leaky gut: mechanisms, measurement and clinical implications in humans,” Gut 68(8), 1516–1526 (2019).
[Crossref]

2017 (5)

R. B. Dorshow, C. Hall-Moore, N. Shaikh, M. R. Talcott, W. A. Faubion, T. E. Rogers, J. J. Shieh, M. P. Debreczeny, J. R. Johnson, R. B. Dyer, R. J. Singh, and P. I. Tarr, “Measurement of gut permeability using fluorescent tracer agent technology,” Sci. Rep. 7(1), 10888 (2017).
[Crossref]

A. Nier, A. J. Engstler, I. B. Maier, and I. Bergheim, “Markers of intestinal permeability are already altered in early stages of non-alcoholic fatty liver disease: Studies in children,” PLoS One 12(9), e0183282 (2017).
[Crossref]

L. Fotis, N. Shaikh, K. W. Baszis, C. M. Samson, R. Lev-Tzion, A. R. French, and P. I. Tarr, “Serologic Evidence of Gut-driven Systemic Inflammation in Juvenile Idiopathic Arthritis,” J. Rheumatol. 44(11), 1624–1631 (2017)..
[Crossref]

C. W. Teshima, K. J. Goodman, M. El-Kalla, S. Turk, W. El-Matary, R. Valcheva, R. Danchak, M. Gordon, P. Ho, A. Mullins, D. Wong, D. Kao, J. Meddings, H. Huynh, and L. A. Dieleman, “Increased Intestinal Permeability in Relatives of Patients With Crohn's Disease Is Not Associated With Small Bowel Ulcerations,” Clin. Gastroenterol. Hepatol. 15(9), 1413–1418.e1 (2017)..
[Crossref]

J. Schleusener, J. Lademann, and M. E. Darvin, “Depth-dependent autofluorescence photobleaching using 325, 473, 633, and 785 nm of porcine ear skin ex vivo,” J. Biomed. Opt. 22(9), 091503 (2017).
[Crossref]

2015 (2)

A. Michielan and R. D’Inca, “Intestinal Permeability in Inflammatory Bowel Disease: Pathogenesis, Clinical Evaluation, and Therapy of Leaky Gut,” Mediators Inflammation 2015, 1–10 (2015).
[Crossref]

B. G. Levesque, W. J. Sandborn, J. Ruel, B. G. Feagan, B. E. Sands, and J. F. Colombel, “Converging goals of treatment of inflammatory bowel disease from clinical trials and practice,” Gastroenterology 148(1), 37–51.e1 (2015).
[Crossref]

2014 (5)

D. M. Denno, K. VanBuskirk, Z. C. Nelson, C. A. Musser, D. C. Hay Burgess, and P. Tarr, “Use of the lactulose to mannitol ratio to evaluate childhood environmental enteric dysfunction: a systematic review,” Clin. Infect. Dis. 59(suppl_4), S213–S219 (2014).
[Crossref]

I. R. Sequeira, R. G. Lentle, M. C. Kruger, and R. D. Hurst, “Standardising the lactulose mannitol test of gut permeability to minimise error and promote comparability,” PLoS One 9(6), e99256 (2014).
[Crossref]

D. T. Rubin, R. Mody, K. L. Davis, and C. C. Wang, “Real-world assessment of therapy changes, suboptimal treatment and associated costs in patients with ulcerative colitis or Crohn's disease,” Aliment. Pharmacol. Ther. 39(10), 1143–1155 (2014).
[Crossref]

S. Shah, M. Akbari, R. Vanga, C. P. Kelly, J. Hansen, T. Theethira, S. Tariq, M. Dennis, and D. A. Leffler, “Patient perception of treatment burden is high in celiac disease compared with other common conditions,” Am. J. Gastroenterol. 109(9), 1304–1311 (2014).
[Crossref]

G. O. Lee, P. Kosek, A. A. M. Lima, R. Singh, P. P. Yori, M. P. Olortegui, J. L. Lamsam, D. B. Oliveira, R. L. Guerrant, and M. Kosek, “Lactulose: mannitol diagnostic test by HPLC and LC-MSMS platforms: considerations for field studies of intestinal barrier function and environmental enteropathy,” J. Pediatr. Gastroenterol. Nutr. 59(4), 544–550 (2014).
[Crossref]

2013 (1)

M. D. Kappelman, K. R. Moore, and J. K. Allen, “Recent Trends in the Prevalence of Crohn’s Disease and Ulcerative Colitis in a Commercially Insured US Population,” Dig. Dis. Sci. 58(2), 519–525 (2013).
[Crossref]

2011 (1)

R. Rajagopalan, W. L. Neumann, A. R. Poreddy, R. M. Fitch, J. N. Freskos, B. Asmelash, K. R. Gaston, K. P. Galen, J. J. Shieh, and R. M. Dorshow, “Hydrophilic pyrazine dyes as exogenous fluorescent tracer agents for real-time point-of-care measurement of glomerular filtration rate,” J. Med. Chem. 54(14), 5048–5058 (2011).
[Crossref]

2008 (1)

A. M. Lostia, L. Lionetto, L. Principessa, M. Evangelisti, A. Gamba, M. P. Villa, and M. Simmaco, “A liquid chromatography/mass spectrometry method for the evaluation of intestinal permeability,” Clin. Biochem. 41(10-11), 887–892 (2008).
[Crossref]

2007 (4)

J. E. Johansson and T. Ekman, “Gut toxicity during hemopoietic stem cell transplantation may predict acute graft-versus-host disease severity in patients,” Dig. Dis. Sci. 52(9), 2340–2345 (2007).
[Crossref]

C. Hesse, V. Razmovski-Naumovski, C. C. Duke, N. M. Davies, and B. D. Roufogalis, “Phytopreventative effects of Gynostemma pentaphyllum against acute Indomethacin-induced gastrointestinal and renal toxicity in rats,” Phytother. Res. 21(6), 523–530 (2007).
[Crossref]

M. Jacob, R. Foster, G. Sigthorsson, R. Simpson, and I. Bjarnason, “Role of bile in pathogenesis of indomethacin-induced enteropathy,” Arch. Toxicol. 81(4), 291–298 (2007)..
[Crossref]

H. Nishio, Y. Hayashi, S. Terashima, and K. Takeuchi, “Protective effect of pranlukast, a cysteinyl-leukotriene receptor 1 antagonist, on indomethacin-induced small intestinal damage in rats,” Inflammopharmacology 15(6), 266–272 (2007).
[Crossref]

2006 (2)

R. S. Bradley and M. S. Thorniley, “A review of attenuation correction techniques for tissue fluorescence,” J. R. Soc., Interface 3(6), 1–13 (2006).
[Crossref]

S. Buhner, C. Buning, J. Genschel, K. Kling, D. Herrmann, A. Dignass, I. Kuechler, S. Krueger, H. H Schmidt, and H. Lochs, “Genetic basis for increased intestinal permeability in families with Crohn's disease: role of CARD15 3020insC mutation,” Gut 55(3), 342–347 (2006).
[Crossref]

2005 (1)

H. Suzuki, N. Hanyou, I. Sonaka, and H. Minami, “An elemental diet controls inflammation in indomethacin-induced small bowel disease in rats: the role of low dietary fat and the elimination of dietary proteins,” Dig. Dis. Sci. 50(10), 1951–1958 (2005).
[Crossref]

2002 (1)

Z. Sun, A. Lasson, K. Olanders, X. Deng, and R. Andersson, “Gut barrier permeability, reticuloendothelial system function and protease inhibitor levels following intestinal ischaemia and reperfusion–effects of pretreatment with N-acetyl-L-cysteine and indomethacin,” Dig. Liver Dis. 34(8), 560–569 (2002).
[Crossref]

1998 (1)

K. Shiraia, A. Yanagisawab, H. Takahashib, K. Fukunishia, and M. Matsuokac, “Syntheses and fluorescent properties of 2,5-diamino-3,6-dicyanopyrazine dyes,” Dyes Pigm. 39(1), 49–68 (1998).
[Crossref]

1997 (3)

M. Peeters, B. Geypens, D. Claus, H. Nevens, Y. Ghoos, G. Verbeke, F. Baert, S. Vermeire, R. Vlietinck, and P. Rutgeerts, “Clustering of increased small intestinal permeability in families with Crohn's disease,” Gastroenterology 113(3), 802–807 (1997).
[Crossref]

E. Smecuol, J. C. Bai, H. Vazquez, Z. Kogan, A. Cabanne, S. Niveloni, S. Pedreira, L. Boerr, E. Mauriño, and J. B. Meddings, “Gastrointestinal permeability in celiac disease,” Gastroenterology 112(4), 1129–1136 (1997).
[Crossref]

M. R. Wright, N. M. Davies, and F. Jamali, “Toxicokinetics of indomethacin-induced intestinal permeability in the rat,” Pharmacol. Res. 35(6), 499–504 (1997).
[Crossref]

1994 (1)

N. M. Davies, M. R. Wright, and F. Jamali, “Antiinflammatory drug-induced small intestinal permeability: the rat is a suitable model,” Pharm. Res. 11(11), 1652–1656 (1994).
[Crossref]

Akbari, M.

S. Shah, M. Akbari, R. Vanga, C. P. Kelly, J. Hansen, T. Theethira, S. Tariq, M. Dennis, and D. A. Leffler, “Patient perception of treatment burden is high in celiac disease compared with other common conditions,” Am. J. Gastroenterol. 109(9), 1304–1311 (2014).
[Crossref]

Allen, J. K.

M. D. Kappelman, K. R. Moore, and J. K. Allen, “Recent Trends in the Prevalence of Crohn’s Disease and Ulcerative Colitis in a Commercially Insured US Population,” Dig. Dis. Sci. 58(2), 519–525 (2013).
[Crossref]

Andersson, R.

Z. Sun, A. Lasson, K. Olanders, X. Deng, and R. Andersson, “Gut barrier permeability, reticuloendothelial system function and protease inhibitor levels following intestinal ischaemia and reperfusion–effects of pretreatment with N-acetyl-L-cysteine and indomethacin,” Dig. Liver Dis. 34(8), 560–569 (2002).
[Crossref]

Asmelash, B.

R. Rajagopalan, W. L. Neumann, A. R. Poreddy, R. M. Fitch, J. N. Freskos, B. Asmelash, K. R. Gaston, K. P. Galen, J. J. Shieh, and R. M. Dorshow, “Hydrophilic pyrazine dyes as exogenous fluorescent tracer agents for real-time point-of-care measurement of glomerular filtration rate,” J. Med. Chem. 54(14), 5048–5058 (2011).
[Crossref]

Baert, F.

M. Peeters, B. Geypens, D. Claus, H. Nevens, Y. Ghoos, G. Verbeke, F. Baert, S. Vermeire, R. Vlietinck, and P. Rutgeerts, “Clustering of increased small intestinal permeability in families with Crohn's disease,” Gastroenterology 113(3), 802–807 (1997).
[Crossref]

Bai, J. C.

E. Smecuol, J. C. Bai, H. Vazquez, Z. Kogan, A. Cabanne, S. Niveloni, S. Pedreira, L. Boerr, E. Mauriño, and J. B. Meddings, “Gastrointestinal permeability in celiac disease,” Gastroenterology 112(4), 1129–1136 (1997).
[Crossref]

Baszis, K. W.

L. Fotis, N. Shaikh, K. W. Baszis, C. M. Samson, R. Lev-Tzion, A. R. French, and P. I. Tarr, “Serologic Evidence of Gut-driven Systemic Inflammation in Juvenile Idiopathic Arthritis,” J. Rheumatol. 44(11), 1624–1631 (2017)..
[Crossref]

Bates, R.

M. P. Debreczeny, R. Bates, R. M. Fitch, K. P. Galen, J. Ge, and R. B. Dorshow, “Human skin auto-fluorescence decay as a function of irradiance and skin type,” Proc. SPIE 7897, Optical Interactions with Tissue and Cells XXII, 78971T (2011).

Bergheim, I.

A. Nier, A. J. Engstler, I. B. Maier, and I. Bergheim, “Markers of intestinal permeability are already altered in early stages of non-alcoholic fatty liver disease: Studies in children,” PLoS One 12(9), e0183282 (2017).
[Crossref]

Bjarnason, I.

M. Jacob, R. Foster, G. Sigthorsson, R. Simpson, and I. Bjarnason, “Role of bile in pathogenesis of indomethacin-induced enteropathy,” Arch. Toxicol. 81(4), 291–298 (2007)..
[Crossref]

Boerr, L.

E. Smecuol, J. C. Bai, H. Vazquez, Z. Kogan, A. Cabanne, S. Niveloni, S. Pedreira, L. Boerr, E. Mauriño, and J. B. Meddings, “Gastrointestinal permeability in celiac disease,” Gastroenterology 112(4), 1129–1136 (1997).
[Crossref]

Bradley, R. S.

R. S. Bradley and M. S. Thorniley, “A review of attenuation correction techniques for tissue fluorescence,” J. R. Soc., Interface 3(6), 1–13 (2006).
[Crossref]

Buhner, S.

S. Buhner, C. Buning, J. Genschel, K. Kling, D. Herrmann, A. Dignass, I. Kuechler, S. Krueger, H. H Schmidt, and H. Lochs, “Genetic basis for increased intestinal permeability in families with Crohn's disease: role of CARD15 3020insC mutation,” Gut 55(3), 342–347 (2006).
[Crossref]

Buning, C.

S. Buhner, C. Buning, J. Genschel, K. Kling, D. Herrmann, A. Dignass, I. Kuechler, S. Krueger, H. H Schmidt, and H. Lochs, “Genetic basis for increased intestinal permeability in families with Crohn's disease: role of CARD15 3020insC mutation,” Gut 55(3), 342–347 (2006).
[Crossref]

Cabanne, A.

E. Smecuol, J. C. Bai, H. Vazquez, Z. Kogan, A. Cabanne, S. Niveloni, S. Pedreira, L. Boerr, E. Mauriño, and J. B. Meddings, “Gastrointestinal permeability in celiac disease,” Gastroenterology 112(4), 1129–1136 (1997).
[Crossref]

Camilleri, M.

M. Camilleri, “Leaky gut: mechanisms, measurement and clinical implications in humans,” Gut 68(8), 1516–1526 (2019).
[Crossref]

Claus, D.

M. Peeters, B. Geypens, D. Claus, H. Nevens, Y. Ghoos, G. Verbeke, F. Baert, S. Vermeire, R. Vlietinck, and P. Rutgeerts, “Clustering of increased small intestinal permeability in families with Crohn's disease,” Gastroenterology 113(3), 802–807 (1997).
[Crossref]

Colombel, J. F.

B. G. Levesque, W. J. Sandborn, J. Ruel, B. G. Feagan, B. E. Sands, and J. F. Colombel, “Converging goals of treatment of inflammatory bowel disease from clinical trials and practice,” Gastroenterology 148(1), 37–51.e1 (2015).
[Crossref]

D’Inca, R.

A. Michielan and R. D’Inca, “Intestinal Permeability in Inflammatory Bowel Disease: Pathogenesis, Clinical Evaluation, and Therapy of Leaky Gut,” Mediators Inflammation 2015, 1–10 (2015).
[Crossref]

Danchak, R.

C. W. Teshima, K. J. Goodman, M. El-Kalla, S. Turk, W. El-Matary, R. Valcheva, R. Danchak, M. Gordon, P. Ho, A. Mullins, D. Wong, D. Kao, J. Meddings, H. Huynh, and L. A. Dieleman, “Increased Intestinal Permeability in Relatives of Patients With Crohn's Disease Is Not Associated With Small Bowel Ulcerations,” Clin. Gastroenterol. Hepatol. 15(9), 1413–1418.e1 (2017)..
[Crossref]

Darvin, M. E.

J. Schleusener, J. Lademann, and M. E. Darvin, “Depth-dependent autofluorescence photobleaching using 325, 473, 633, and 785 nm of porcine ear skin ex vivo,” J. Biomed. Opt. 22(9), 091503 (2017).
[Crossref]

Davies, N. M.

C. Hesse, V. Razmovski-Naumovski, C. C. Duke, N. M. Davies, and B. D. Roufogalis, “Phytopreventative effects of Gynostemma pentaphyllum against acute Indomethacin-induced gastrointestinal and renal toxicity in rats,” Phytother. Res. 21(6), 523–530 (2007).
[Crossref]

M. R. Wright, N. M. Davies, and F. Jamali, “Toxicokinetics of indomethacin-induced intestinal permeability in the rat,” Pharmacol. Res. 35(6), 499–504 (1997).
[Crossref]

N. M. Davies, M. R. Wright, and F. Jamali, “Antiinflammatory drug-induced small intestinal permeability: the rat is a suitable model,” Pharm. Res. 11(11), 1652–1656 (1994).
[Crossref]

Davis, K. L.

D. T. Rubin, R. Mody, K. L. Davis, and C. C. Wang, “Real-world assessment of therapy changes, suboptimal treatment and associated costs in patients with ulcerative colitis or Crohn's disease,” Aliment. Pharmacol. Ther. 39(10), 1143–1155 (2014).
[Crossref]

Debreczeny, M. P.

R. B. Dorshow, C. Hall-Moore, N. Shaikh, M. R. Talcott, W. A. Faubion, T. E. Rogers, J. J. Shieh, M. P. Debreczeny, J. R. Johnson, R. B. Dyer, R. J. Singh, and P. I. Tarr, “Measurement of gut permeability using fluorescent tracer agent technology,” Sci. Rep. 7(1), 10888 (2017).
[Crossref]

M. P. Debreczeny, R. Bates, R. M. Fitch, K. P. Galen, J. Ge, and R. B. Dorshow, “Human skin auto-fluorescence decay as a function of irradiance and skin type,” Proc. SPIE 7897, Optical Interactions with Tissue and Cells XXII, 78971T (2011).

Deng, X.

Z. Sun, A. Lasson, K. Olanders, X. Deng, and R. Andersson, “Gut barrier permeability, reticuloendothelial system function and protease inhibitor levels following intestinal ischaemia and reperfusion–effects of pretreatment with N-acetyl-L-cysteine and indomethacin,” Dig. Liver Dis. 34(8), 560–569 (2002).
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S. Shah, M. Akbari, R. Vanga, C. P. Kelly, J. Hansen, T. Theethira, S. Tariq, M. Dennis, and D. A. Leffler, “Patient perception of treatment burden is high in celiac disease compared with other common conditions,” Am. J. Gastroenterol. 109(9), 1304–1311 (2014).
[Crossref]

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D. M. Denno, K. VanBuskirk, Z. C. Nelson, C. A. Musser, D. C. Hay Burgess, and P. Tarr, “Use of the lactulose to mannitol ratio to evaluate childhood environmental enteric dysfunction: a systematic review,” Clin. Infect. Dis. 59(suppl_4), S213–S219 (2014).
[Crossref]

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C. W. Teshima, K. J. Goodman, M. El-Kalla, S. Turk, W. El-Matary, R. Valcheva, R. Danchak, M. Gordon, P. Ho, A. Mullins, D. Wong, D. Kao, J. Meddings, H. Huynh, and L. A. Dieleman, “Increased Intestinal Permeability in Relatives of Patients With Crohn's Disease Is Not Associated With Small Bowel Ulcerations,” Clin. Gastroenterol. Hepatol. 15(9), 1413–1418.e1 (2017)..
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S. Buhner, C. Buning, J. Genschel, K. Kling, D. Herrmann, A. Dignass, I. Kuechler, S. Krueger, H. H Schmidt, and H. Lochs, “Genetic basis for increased intestinal permeability in families with Crohn's disease: role of CARD15 3020insC mutation,” Gut 55(3), 342–347 (2006).
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R. B. Dorshow, C. Hall-Moore, N. Shaikh, M. R. Talcott, W. A. Faubion, T. E. Rogers, J. J. Shieh, M. P. Debreczeny, J. R. Johnson, R. B. Dyer, R. J. Singh, and P. I. Tarr, “Measurement of gut permeability using fluorescent tracer agent technology,” Sci. Rep. 7(1), 10888 (2017).
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M. P. Debreczeny, R. Bates, R. M. Fitch, K. P. Galen, J. Ge, and R. B. Dorshow, “Human skin auto-fluorescence decay as a function of irradiance and skin type,” Proc. SPIE 7897, Optical Interactions with Tissue and Cells XXII, 78971T (2011).

Dorshow, R. M.

R. Rajagopalan, W. L. Neumann, A. R. Poreddy, R. M. Fitch, J. N. Freskos, B. Asmelash, K. R. Gaston, K. P. Galen, J. J. Shieh, and R. M. Dorshow, “Hydrophilic pyrazine dyes as exogenous fluorescent tracer agents for real-time point-of-care measurement of glomerular filtration rate,” J. Med. Chem. 54(14), 5048–5058 (2011).
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C. Hesse, V. Razmovski-Naumovski, C. C. Duke, N. M. Davies, and B. D. Roufogalis, “Phytopreventative effects of Gynostemma pentaphyllum against acute Indomethacin-induced gastrointestinal and renal toxicity in rats,” Phytother. Res. 21(6), 523–530 (2007).
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R. B. Dorshow, C. Hall-Moore, N. Shaikh, M. R. Talcott, W. A. Faubion, T. E. Rogers, J. J. Shieh, M. P. Debreczeny, J. R. Johnson, R. B. Dyer, R. J. Singh, and P. I. Tarr, “Measurement of gut permeability using fluorescent tracer agent technology,” Sci. Rep. 7(1), 10888 (2017).
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C. W. Teshima, K. J. Goodman, M. El-Kalla, S. Turk, W. El-Matary, R. Valcheva, R. Danchak, M. Gordon, P. Ho, A. Mullins, D. Wong, D. Kao, J. Meddings, H. Huynh, and L. A. Dieleman, “Increased Intestinal Permeability in Relatives of Patients With Crohn's Disease Is Not Associated With Small Bowel Ulcerations,” Clin. Gastroenterol. Hepatol. 15(9), 1413–1418.e1 (2017)..
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C. W. Teshima, K. J. Goodman, M. El-Kalla, S. Turk, W. El-Matary, R. Valcheva, R. Danchak, M. Gordon, P. Ho, A. Mullins, D. Wong, D. Kao, J. Meddings, H. Huynh, and L. A. Dieleman, “Increased Intestinal Permeability in Relatives of Patients With Crohn's Disease Is Not Associated With Small Bowel Ulcerations,” Clin. Gastroenterol. Hepatol. 15(9), 1413–1418.e1 (2017)..
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R. B. Dorshow, C. Hall-Moore, N. Shaikh, M. R. Talcott, W. A. Faubion, T. E. Rogers, J. J. Shieh, M. P. Debreczeny, J. R. Johnson, R. B. Dyer, R. J. Singh, and P. I. Tarr, “Measurement of gut permeability using fluorescent tracer agent technology,” Sci. Rep. 7(1), 10888 (2017).
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B. G. Levesque, W. J. Sandborn, J. Ruel, B. G. Feagan, B. E. Sands, and J. F. Colombel, “Converging goals of treatment of inflammatory bowel disease from clinical trials and practice,” Gastroenterology 148(1), 37–51.e1 (2015).
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R. Rajagopalan, W. L. Neumann, A. R. Poreddy, R. M. Fitch, J. N. Freskos, B. Asmelash, K. R. Gaston, K. P. Galen, J. J. Shieh, and R. M. Dorshow, “Hydrophilic pyrazine dyes as exogenous fluorescent tracer agents for real-time point-of-care measurement of glomerular filtration rate,” J. Med. Chem. 54(14), 5048–5058 (2011).
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M. P. Debreczeny, R. Bates, R. M. Fitch, K. P. Galen, J. Ge, and R. B. Dorshow, “Human skin auto-fluorescence decay as a function of irradiance and skin type,” Proc. SPIE 7897, Optical Interactions with Tissue and Cells XXII, 78971T (2011).

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M. Jacob, R. Foster, G. Sigthorsson, R. Simpson, and I. Bjarnason, “Role of bile in pathogenesis of indomethacin-induced enteropathy,” Arch. Toxicol. 81(4), 291–298 (2007)..
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L. Fotis, N. Shaikh, K. W. Baszis, C. M. Samson, R. Lev-Tzion, A. R. French, and P. I. Tarr, “Serologic Evidence of Gut-driven Systemic Inflammation in Juvenile Idiopathic Arthritis,” J. Rheumatol. 44(11), 1624–1631 (2017)..
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M. P. Debreczeny, R. Bates, R. M. Fitch, K. P. Galen, J. Ge, and R. B. Dorshow, “Human skin auto-fluorescence decay as a function of irradiance and skin type,” Proc. SPIE 7897, Optical Interactions with Tissue and Cells XXII, 78971T (2011).

Gamba, A.

A. M. Lostia, L. Lionetto, L. Principessa, M. Evangelisti, A. Gamba, M. P. Villa, and M. Simmaco, “A liquid chromatography/mass spectrometry method for the evaluation of intestinal permeability,” Clin. Biochem. 41(10-11), 887–892 (2008).
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R. Rajagopalan, W. L. Neumann, A. R. Poreddy, R. M. Fitch, J. N. Freskos, B. Asmelash, K. R. Gaston, K. P. Galen, J. J. Shieh, and R. M. Dorshow, “Hydrophilic pyrazine dyes as exogenous fluorescent tracer agents for real-time point-of-care measurement of glomerular filtration rate,” J. Med. Chem. 54(14), 5048–5058 (2011).
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M. P. Debreczeny, R. Bates, R. M. Fitch, K. P. Galen, J. Ge, and R. B. Dorshow, “Human skin auto-fluorescence decay as a function of irradiance and skin type,” Proc. SPIE 7897, Optical Interactions with Tissue and Cells XXII, 78971T (2011).

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S. Buhner, C. Buning, J. Genschel, K. Kling, D. Herrmann, A. Dignass, I. Kuechler, S. Krueger, H. H Schmidt, and H. Lochs, “Genetic basis for increased intestinal permeability in families with Crohn's disease: role of CARD15 3020insC mutation,” Gut 55(3), 342–347 (2006).
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C. W. Teshima, K. J. Goodman, M. El-Kalla, S. Turk, W. El-Matary, R. Valcheva, R. Danchak, M. Gordon, P. Ho, A. Mullins, D. Wong, D. Kao, J. Meddings, H. Huynh, and L. A. Dieleman, “Increased Intestinal Permeability in Relatives of Patients With Crohn's Disease Is Not Associated With Small Bowel Ulcerations,” Clin. Gastroenterol. Hepatol. 15(9), 1413–1418.e1 (2017)..
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R. B. Dorshow, C. Hall-Moore, N. Shaikh, M. R. Talcott, W. A. Faubion, T. E. Rogers, J. J. Shieh, M. P. Debreczeny, J. R. Johnson, R. B. Dyer, R. J. Singh, and P. I. Tarr, “Measurement of gut permeability using fluorescent tracer agent technology,” Sci. Rep. 7(1), 10888 (2017).
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S. Shah, M. Akbari, R. Vanga, C. P. Kelly, J. Hansen, T. Theethira, S. Tariq, M. Dennis, and D. A. Leffler, “Patient perception of treatment burden is high in celiac disease compared with other common conditions,” Am. J. Gastroenterol. 109(9), 1304–1311 (2014).
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D. M. Denno, K. VanBuskirk, Z. C. Nelson, C. A. Musser, D. C. Hay Burgess, and P. Tarr, “Use of the lactulose to mannitol ratio to evaluate childhood environmental enteric dysfunction: a systematic review,” Clin. Infect. Dis. 59(suppl_4), S213–S219 (2014).
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C. Hesse, V. Razmovski-Naumovski, C. C. Duke, N. M. Davies, and B. D. Roufogalis, “Phytopreventative effects of Gynostemma pentaphyllum against acute Indomethacin-induced gastrointestinal and renal toxicity in rats,” Phytother. Res. 21(6), 523–530 (2007).
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C. W. Teshima, K. J. Goodman, M. El-Kalla, S. Turk, W. El-Matary, R. Valcheva, R. Danchak, M. Gordon, P. Ho, A. Mullins, D. Wong, D. Kao, J. Meddings, H. Huynh, and L. A. Dieleman, “Increased Intestinal Permeability in Relatives of Patients With Crohn's Disease Is Not Associated With Small Bowel Ulcerations,” Clin. Gastroenterol. Hepatol. 15(9), 1413–1418.e1 (2017)..
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I. R. Sequeira, R. G. Lentle, M. C. Kruger, and R. D. Hurst, “Standardising the lactulose mannitol test of gut permeability to minimise error and promote comparability,” PLoS One 9(6), e99256 (2014).
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C. W. Teshima, K. J. Goodman, M. El-Kalla, S. Turk, W. El-Matary, R. Valcheva, R. Danchak, M. Gordon, P. Ho, A. Mullins, D. Wong, D. Kao, J. Meddings, H. Huynh, and L. A. Dieleman, “Increased Intestinal Permeability in Relatives of Patients With Crohn's Disease Is Not Associated With Small Bowel Ulcerations,” Clin. Gastroenterol. Hepatol. 15(9), 1413–1418.e1 (2017)..
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M. Jacob, R. Foster, G. Sigthorsson, R. Simpson, and I. Bjarnason, “Role of bile in pathogenesis of indomethacin-induced enteropathy,” Arch. Toxicol. 81(4), 291–298 (2007)..
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J. E. Johansson and T. Ekman, “Gut toxicity during hemopoietic stem cell transplantation may predict acute graft-versus-host disease severity in patients,” Dig. Dis. Sci. 52(9), 2340–2345 (2007).
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R. B. Dorshow, C. Hall-Moore, N. Shaikh, M. R. Talcott, W. A. Faubion, T. E. Rogers, J. J. Shieh, M. P. Debreczeny, J. R. Johnson, R. B. Dyer, R. J. Singh, and P. I. Tarr, “Measurement of gut permeability using fluorescent tracer agent technology,” Sci. Rep. 7(1), 10888 (2017).
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C. W. Teshima, K. J. Goodman, M. El-Kalla, S. Turk, W. El-Matary, R. Valcheva, R. Danchak, M. Gordon, P. Ho, A. Mullins, D. Wong, D. Kao, J. Meddings, H. Huynh, and L. A. Dieleman, “Increased Intestinal Permeability in Relatives of Patients With Crohn's Disease Is Not Associated With Small Bowel Ulcerations,” Clin. Gastroenterol. Hepatol. 15(9), 1413–1418.e1 (2017)..
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G. O. Lee, P. Kosek, A. A. M. Lima, R. Singh, P. P. Yori, M. P. Olortegui, J. L. Lamsam, D. B. Oliveira, R. L. Guerrant, and M. Kosek, “Lactulose: mannitol diagnostic test by HPLC and LC-MSMS platforms: considerations for field studies of intestinal barrier function and environmental enteropathy,” J. Pediatr. Gastroenterol. Nutr. 59(4), 544–550 (2014).
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S. Buhner, C. Buning, J. Genschel, K. Kling, D. Herrmann, A. Dignass, I. Kuechler, S. Krueger, H. H Schmidt, and H. Lochs, “Genetic basis for increased intestinal permeability in families with Crohn's disease: role of CARD15 3020insC mutation,” Gut 55(3), 342–347 (2006).
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I. R. Sequeira, R. G. Lentle, M. C. Kruger, and R. D. Hurst, “Standardising the lactulose mannitol test of gut permeability to minimise error and promote comparability,” PLoS One 9(6), e99256 (2014).
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Kuechler, I.

S. Buhner, C. Buning, J. Genschel, K. Kling, D. Herrmann, A. Dignass, I. Kuechler, S. Krueger, H. H Schmidt, and H. Lochs, “Genetic basis for increased intestinal permeability in families with Crohn's disease: role of CARD15 3020insC mutation,” Gut 55(3), 342–347 (2006).
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Lasson, A.

Z. Sun, A. Lasson, K. Olanders, X. Deng, and R. Andersson, “Gut barrier permeability, reticuloendothelial system function and protease inhibitor levels following intestinal ischaemia and reperfusion–effects of pretreatment with N-acetyl-L-cysteine and indomethacin,” Dig. Liver Dis. 34(8), 560–569 (2002).
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G. O. Lee, P. Kosek, A. A. M. Lima, R. Singh, P. P. Yori, M. P. Olortegui, J. L. Lamsam, D. B. Oliveira, R. L. Guerrant, and M. Kosek, “Lactulose: mannitol diagnostic test by HPLC and LC-MSMS platforms: considerations for field studies of intestinal barrier function and environmental enteropathy,” J. Pediatr. Gastroenterol. Nutr. 59(4), 544–550 (2014).
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S. Shah, M. Akbari, R. Vanga, C. P. Kelly, J. Hansen, T. Theethira, S. Tariq, M. Dennis, and D. A. Leffler, “Patient perception of treatment burden is high in celiac disease compared with other common conditions,” Am. J. Gastroenterol. 109(9), 1304–1311 (2014).
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I. R. Sequeira, R. G. Lentle, M. C. Kruger, and R. D. Hurst, “Standardising the lactulose mannitol test of gut permeability to minimise error and promote comparability,” PLoS One 9(6), e99256 (2014).
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L. Fotis, N. Shaikh, K. W. Baszis, C. M. Samson, R. Lev-Tzion, A. R. French, and P. I. Tarr, “Serologic Evidence of Gut-driven Systemic Inflammation in Juvenile Idiopathic Arthritis,” J. Rheumatol. 44(11), 1624–1631 (2017)..
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G. O. Lee, P. Kosek, A. A. M. Lima, R. Singh, P. P. Yori, M. P. Olortegui, J. L. Lamsam, D. B. Oliveira, R. L. Guerrant, and M. Kosek, “Lactulose: mannitol diagnostic test by HPLC and LC-MSMS platforms: considerations for field studies of intestinal barrier function and environmental enteropathy,” J. Pediatr. Gastroenterol. Nutr. 59(4), 544–550 (2014).
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S. Buhner, C. Buning, J. Genschel, K. Kling, D. Herrmann, A. Dignass, I. Kuechler, S. Krueger, H. H Schmidt, and H. Lochs, “Genetic basis for increased intestinal permeability in families with Crohn's disease: role of CARD15 3020insC mutation,” Gut 55(3), 342–347 (2006).
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A. M. Lostia, L. Lionetto, L. Principessa, M. Evangelisti, A. Gamba, M. P. Villa, and M. Simmaco, “A liquid chromatography/mass spectrometry method for the evaluation of intestinal permeability,” Clin. Biochem. 41(10-11), 887–892 (2008).
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E. Smecuol, J. C. Bai, H. Vazquez, Z. Kogan, A. Cabanne, S. Niveloni, S. Pedreira, L. Boerr, E. Mauriño, and J. B. Meddings, “Gastrointestinal permeability in celiac disease,” Gastroenterology 112(4), 1129–1136 (1997).
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M. Peeters, B. Geypens, D. Claus, H. Nevens, Y. Ghoos, G. Verbeke, F. Baert, S. Vermeire, R. Vlietinck, and P. Rutgeerts, “Clustering of increased small intestinal permeability in families with Crohn's disease,” Gastroenterology 113(3), 802–807 (1997).
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G. O. Lee, P. Kosek, A. A. M. Lima, R. Singh, P. P. Yori, M. P. Olortegui, J. L. Lamsam, D. B. Oliveira, R. L. Guerrant, and M. Kosek, “Lactulose: mannitol diagnostic test by HPLC and LC-MSMS platforms: considerations for field studies of intestinal barrier function and environmental enteropathy,” J. Pediatr. Gastroenterol. Nutr. 59(4), 544–550 (2014).
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Figures (9)

Fig. 1.
Fig. 1. MB-301 (left) and MB-404 (right) structural diagrams.
Fig. 2.
Fig. 2. Experimental set-up for in vivo transdermal fluorescence acquisition and urine collection.
Fig. 3.
Fig. 3. Transdermal fluorescence detection system schematic illustrating the illumination system and one of four identical detection channels. (Filter center wavelengths given with full width at half maximum bandwidth (FWHM).)
Fig. 4.
Fig. 4. Calibration of MB-404 and MB-301 in 1% Intralipid across the 4 detection channels. Blue squares are the data points for the 400 nm excitation and the red circles are the data points for the 500 nm excitation. Dashed lines are linear regressions.
Fig. 5.
Fig. 5. MB-404% recovery in Rat Urine. Blue bars are injured rats, red bars are control rats.
Fig. 6.
Fig. 6. MB-301 recovery in Rat Urine. Blue bars are injured rats, red bars are control rats.
Fig. 7.
Fig. 7. (a). Concentration time-course of MB-404 derived from transdermal fluorophore intensity measurements at 593 nm (with 505 nm excitation). Solid lines represent injured rats, dashed lines represent control rats. Time zero represents the time of gavage. (b). Concentration time-course of MB-301 derived from transdermal fluorophore intensity measurements at 540 nm (with 402 nm excitation). Solid lines represent injured rats, dashed lines represent control rats. Time zero represents the time of gavage.
Fig. 8.
Fig. 8. MB-404/MB-301 Ratio of concentration vs time. Solid lines represent the injured rats, dashed lines represent the control rats.
Fig. 9.
Fig. 9. MB-404/MB-301 AUC Ratio of concentration vs time. Solid lines represent the injured rats, dashed lines represent the control rats. (The units for AUC for each compound are wt/vol * hour. The ratio is of course dimensionless.)

Tables (3)

Tables Icon

Table 1. Discrimination Error Estimates for Optically Determined Concentrations.

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Table 2. Parameters, analysis, and results of fluorophore recovery in urine samples. Blue indicates injured rats, red indicates control rats.

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Table 3. Average (with standard deviation) percent recovery of fluorophore and p-value from two-sample t-test of injured to control.

Equations (2)

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E L = 100 C L ( H + L ) C L ( L o n l y ) C L ( L o n l y )
E H = 100 C H ( H + L ) C H ( H o n l y ) C H ( H o n l y )

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