A neurobiological link between transportation noise exposure and metabolic disease in humans

Michael T Osborne¹, Nicki Naddaf², Shady Abohashem³, Azar Radfar⁴, Ahmed Ghoneem⁵, Tawseef Dar⁶, Ying Wang⁷, Tomas Patrich⁸, Blake Oberfeld⁹, Brian Tung¹⁰, Roger K Pitman¹¹, Nehal N Mehta¹², Lisa M Shin¹³, Janet Lo¹⁴, Sanjay Rajagopalan¹⁵, Karestan C Koenen¹⁶, Steven K Grinspoon¹⁷, Zahi A Fayad¹⁸, Ahmed Tawakol¹⁹

Affiliations

¹ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA; Cardiology Division, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: mosborne@mgh.harvard.edu.
² Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA. Electronic address: nicki.naddaf@stonybrookmedicine.edu.
³ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA; Cardiology Division, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: sabohashem@mgh.harvard.edu.
⁴ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA; Cardiology Division, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: azar.radfar@jhsmiami.org.
⁵ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA. Electronic address: ahmed.ghoneem@lahey.org.
⁶ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA; Cardiology Division, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: tawseef.dar@jhsmiami.org.
⁷ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA. Electronic address: ywang88@mgh.harvard.edu.
⁸ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA. Electronic address: tomy@patrich.com.
⁹ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA. Electronic address: blake_oberfeld@hms.harvard.edu.
¹⁰ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA. Electronic address: btung@student.nymc.edu.
¹¹ Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: roger_pitman@hms.harvard.edu.
¹² Section of Inflammation and Cardiometabolic Diseases, National Heart, Lung, and Blood Institute, National Institutes of Health, 10 Center Dr., Building 10, Room 5-5140, Bethesda, MD 02814, USA. Electronic address: nehal.mehta@nih.gov.
¹³ Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA; Department of Psychology, Tufts University, 490 Boston Ave., Medford, MA 02155, USA. Electronic address: lisa.shin@tufts.edu.
¹⁴ Neuroendocrine Unit, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: jlo@mgh.harvard.edu.
¹⁵ Department of Cardiovascular Medicine, Case Western Reserve University, 11100 Euclid Ave., Cleveland, OH 44106, USA. Electronic address: sxr647@case.edu.
¹⁶ Department of Epidemiology, Harvard University T.H. Chan School of Public Health, 677 Huntington Ave., Kresge Building, 505, Boston, MA 02115, USA. Electronic address: kkoenen@hsph.harvard.edu.
¹⁷ Neuroendocrine Unit, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: sgrinspoon@mgh.harvard.edu.
¹⁸ BioMedical Engineering and Imaging Institute, Icahn School of Medicine at Mount Sinai, 1470 Madison Ave., New York, NY 10029, USA. Electronic address: zahi.fayad@mssm.edu.
¹⁹ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA; Cardiology Division, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: atawakol@mgh.harvard.edu.

PMID: 34183223
PMCID: PMC8405593
DOI: 10.1016/j.psyneuen.2021.105331

A neurobiological link between transportation noise exposure and metabolic disease in humans

Michael T Osborne et al. Psychoneuroendocrinology. 2021 Sep.

. 2021 Sep:131:105331.

doi: 10.1016/j.psyneuen.2021.105331. Epub 2021 Jun 17.

Authors

Affiliations

¹ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA; Cardiology Division, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: mosborne@mgh.harvard.edu.
² Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA. Electronic address: nicki.naddaf@stonybrookmedicine.edu.
³ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA; Cardiology Division, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: sabohashem@mgh.harvard.edu.
⁴ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA; Cardiology Division, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: azar.radfar@jhsmiami.org.
⁵ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA. Electronic address: ahmed.ghoneem@lahey.org.
⁶ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA; Cardiology Division, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: tawseef.dar@jhsmiami.org.
⁷ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA. Electronic address: ywang88@mgh.harvard.edu.
⁸ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA. Electronic address: tomy@patrich.com.
⁹ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA. Electronic address: blake_oberfeld@hms.harvard.edu.
¹⁰ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA. Electronic address: btung@student.nymc.edu.
¹¹ Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: roger_pitman@hms.harvard.edu.
¹² Section of Inflammation and Cardiometabolic Diseases, National Heart, Lung, and Blood Institute, National Institutes of Health, 10 Center Dr., Building 10, Room 5-5140, Bethesda, MD 02814, USA. Electronic address: nehal.mehta@nih.gov.
¹³ Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA; Department of Psychology, Tufts University, 490 Boston Ave., Medford, MA 02155, USA. Electronic address: lisa.shin@tufts.edu.
¹⁴ Neuroendocrine Unit, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: jlo@mgh.harvard.edu.
¹⁵ Department of Cardiovascular Medicine, Case Western Reserve University, 11100 Euclid Ave., Cleveland, OH 44106, USA. Electronic address: sxr647@case.edu.
¹⁶ Department of Epidemiology, Harvard University T.H. Chan School of Public Health, 677 Huntington Ave., Kresge Building, 505, Boston, MA 02115, USA. Electronic address: kkoenen@hsph.harvard.edu.
¹⁷ Neuroendocrine Unit, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: sgrinspoon@mgh.harvard.edu.
¹⁸ BioMedical Engineering and Imaging Institute, Icahn School of Medicine at Mount Sinai, 1470 Madison Ave., New York, NY 10029, USA. Electronic address: zahi.fayad@mssm.edu.
¹⁹ Cardiac Imaging Research Center, Massachusetts General Hospital, 165 Cambridge St., Suite 400, Boston, MA 02114, USA; Cardiology Division, Massachusetts General Hospital and Harvard Medical School, 55 Fruit St., Boston, MA 02114, USA. Electronic address: atawakol@mgh.harvard.edu.

PMID: 34183223
PMCID: PMC8405593
DOI: 10.1016/j.psyneuen.2021.105331

Abstract

Background: Chronic transportation noise exposure associates with cardiovascular events through a link involving heightened stress-associated neurobiological activity (as amygdalar metabolic activity, AmygA) on ¹⁸F-fluorodeoxyglucose positron emission tomography/computed tomography (¹⁸F-FDG-PET/CT). Increased AmygA also associates with greater visceral adipose tissue (VAT) and type 2 diabetes mellitus (DM). While relationships between noise exposure and VAT and DM have been reported, the underlying mechanisms remain incompletely understood. We tested whether: (1) transportation noise exposure associates with greater (a) baseline and gains in VAT and (b) DM risk, and (2) heightened AmygA partially mediates the link between noise exposure and these metabolic diseases.

Methods: VAT was measured in a retrospective cohort (N = 403) who underwent clinical ¹⁸F-FDG-PET/CT. AmygA was measured in those with brain imaging (N = 238). Follow-up VAT was remeasured on available imaging (N = 67). Among individuals (N = 224) without baseline DM, incident DM was adjudicated over 2 years from clinical records. Noise (24-h average) was modeled at each individual's home address. Linear regression, survival, and mediation analyses were employed.

Results: Higher noise exposure (upper tertile vs. others) associated with greater: baseline VAT (standardized β [95% confidence interval (CI)]= 0.230 [0.021, 0.438], p = 0.031), gains in VAT (0.686 [0.185, 1.187], p = 0.008 adjusted for baseline VAT), and DM (hazard ratio [95% CI]=2.429 [1.031, 5.719], p = 0.042). The paths of: ↑noise exposure→↑AmygA→↑baseline VAT and ↑noise exposure→↑AmygA→↑subsequent DM were significant (p < 0.05).

Conclusions: Increased transportation noise exposure associates with greater VAT and DM. This relationship is partially mediated by stress-associated neurobiological activity. These findings suggest altered neurobiology contributes to noise exposure's link to metabolic diseases.

Keywords: Amygdalar activity; Diabetes mellitus; Noise exposure; Positron emission tomography; Visceral adiposity.

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Conflict of interest statement

Declaration of Interests

Michael Osborne, MD received consulting fees from Intrinsic Imaging, LLC for unrelated work. Steven K. Grinspoon, MD received consulting fees from Viiv and Theratechnologies for unrelated work. Ahmed Tawakol, MD received institutional grants from Genentech and personal fees from Actelion, DalCor, Cor2ed, and Esperion for unrelated research. The remaining authors have no significant disclosures.

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Figures

**Figure 1:**
Patient selection for the adiposity and DM samples. Abbreviations: CVD-cardiovascular disease, DM-diabetes mellitus, FDG PET/CT-fluorodeoxyglucose positron emission tomography/computed tomography, HTN-hypertension, VAT-visceral adipose tissue.

**Figure 2:**
Kaplan-Meier plot of type 2 DM-free survival by transportation noise exposure (upper tertile or >45 dBA vs. others). Log-rank p-value and a multivariable Cox model adjusted for age and sex are shown. Abbreviations: CI-confidence interval, DM-diabetes mellitus, HR-hazard ratio.

**Figure 3:**
Mediation models evaluating the pathways linking increased transportation noise exposure (>45 dBA) to: A) increased VAT through increased amygdalar metabolic activity and B) increased type 2 DM risk through increased amygdalar metabolic activity. Models are unadjusted. Indirect pathways are shown in red and direct pathways are shown in black. Abbreviations: AmygA-amygdalar metabolic activity, CI-confidence interval, VAT-visceral adipose tissue.

See this image and copyright information in PMC

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A neurobiological link between transportation noise exposure and metabolic disease in humans

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A neurobiological link between transportation noise exposure and metabolic disease in humans

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Conflict of interest statement

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