Pupillary Light Reflexes are Associated with Autonomic Dysfunction in Bolivian Diabetics But Not Chagas Disease Patients

Anthony Halperin Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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Monica Pajuelo Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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Jeffrey A. Tornheim Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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Nancy Vu Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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Andrés M. Carnero Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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Gerson Galdos-Cardenas Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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Lisbeth Ferrufino Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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Marilyn Camacho Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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Juan Justiniano Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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Rony Colanzi Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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Natalie M. Bowman Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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Tiffany Morris Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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Hamish MacDougall Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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Caryn Bern Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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Steven T. Moore Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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Robert H. Gilman Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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the Chagas Working Group in Bolivia and Peru Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru; Combined Internal Medicine and Pediatrics Residency Program, Yale School of Medicine, New Haven, Connecticut; University of Utah, Salt Lake City, Utah; Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland; Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia; Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina; Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York; School of Psychology, University of Sydney, Sydney, Australia; Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, California

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DOI:
https://doi.org/10.4269/ajtmh.14-0775
Volume/Issue:
Volume 94: Issue 6
Page(s):
1290–1298
Restricted access
Get Permissions

Autonomic dysfunction is common in Chagas disease and diabetes. Patients with either condition complicated by cardiac autonomic dysfunction face increased mortality, but no clinical predictors of autonomic dysfunction exist. Pupillary light reflexes (PLRs) may identify such patients early, allowing for intensified treatment. To evaluate the significance of PLRs, adults were recruited from the outpatient endocrine, cardiology, and surgical clinics at a Bolivian teaching hospital. After testing for Chagas disease and diabetes, participants completed conventional autonomic testing (CAT) evaluating their cardiovascular responses to Valsalva, deep breathing, and orthostatic changes. PLRs were measured using specially designed goggles, then CAT and PLRs were compared as measures of autonomic dysfunction. This study analyzed 163 adults, including 96 with Chagas disease, 35 patients with diabetes, and 32 controls. PLRs were not significantly different between Chagas disease patients and controls. Patients with diabetes had longer latency to onset of pupil constriction, slower maximum constriction velocities, and smaller orthostatic ratios than nonpatients with diabetes. PLRs correlated poorly with CAT results. A PLR-based clinical risk score demonstrated a 2.27-fold increased likelihood of diabetes complicated by autonomic dysfunction compared with the combination of blood tests, CAT, and PLRs (sensitivity 87.9%, specificity 61.3%). PLRs represent a promising tool for evaluating subclinical neuropathy in patients with diabetes without symptomatic autonomic dysfunction. Pupillometry does not have a role in the evaluation of Chagas disease patients.

Author Notes

* Address correspondences to Jeffrey A. Tornheim, Division of Infectious Diseases, The Johns Hopkins University School of Medicine, 1830 E. Monument Street, Room 450C, Baltimore, MD 21287. E-mail: tornheim@jhu.edu
† These authors contributed equally to this work.
‡ Deceased.

Financial support: This work was supported by the National Institutes of Health Fogarty International Clinical Scholars Program. Additional funding for pupillometer development and salary support for Drs. Moore and Morris was provided by National Aeronautics and Space Administration grant NNX12AM25G.

Authors' addresses: Anthony Halperin, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA. Monica Pajuelo, Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mail: mjpajuelo@gmail.com. Jeffrey A. Tornheim, Division of Infectious Diseases, The Johns Hopkins University School of Medicine, Baltimore, MD, E-mail: tornheim@jhu.edu. Nancy Vu, Internal Medicine Residency Program, Cleveland Clinic, Cleveland, OH, E-mail: nancy.mary.vu@gmail.com. Andrés M. Carnero, Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mail: andrescarnero@gmail.com. Gerson Galdos-Cardenas, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, and Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia, E-mail: gerson_galdos@yahoo.es. Lisbeth Ferrufino, Clinical Laboratory, Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia, E-mail: lisbeth_ferrufino@yahoo.es. Marilyn Camacho, Department of Internal Medicine, Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia, E-mail: marilincamachoa@hotmail.com. Juan Justiniano, Department of Cardiology, Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia, E-mail: juanjustiniano@hotmail.com. Rony Colanzi, Department of Pathology, Hospital Universitario Japonés, Santa Cruz de la Sierra, Bolivia, and Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia, E-mail: ronycolanzi@hotmail.com. Natalie M. Bowman, Division of Infectious Disease, Department of Medicine, University of North Carolina, Chapel Hill, NC, E-mail: natalie.bowman@gmail.com. Tiffany Morris, Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, NY, E-mail: tiffanyrmorris@gmail.com. Hamish MacDougall, School of Psychology, University of Sydney, Australia, E-mail: hamish@psych.usyd.edu.au. Caryn Bern, Division of Epidemiology and Biostatistics, University of California San Francisco School of Medicine, San Francisco, CA, E-mail: Caryn.Bern2@ucsf.edu. Steven T. Moore, Department of Neurology, Icahn School of Medicine at Mount Sinai, New York City, NY, E-mail: steven.moore@mssm.edu. Robert H. Gilman, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, and Laboratory of Infectious Diseases Research, Universidad Peruana Cayetano Heredia, Lima, Peru, and Universidad Católica Boliviana “San Pablo,” Santa Cruz de la Sierra, Bolivia, E-mail: rgilman@jhsph.edu.

Copyright:
© The American Society of Tropical Medicine and Hygiene 2016
Received:
02 Dec 2014
|
Accepted:
16 Jan 2016
|
Published Online:
01 Jun 2016
Cover The American Journal of Tropical Medicine and Hygiene
The American Journal of Tropical Medicine and Hygiene
Print ISSN:
0002-9637
Online ISSN:
1476-1645
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