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Metabolomic, hormonal and physiological responses to hypoglycemia versus euglycemia during exercise in adults with type 1 diabetes

Olivia McCarthy, Jason Pitt, Rachel Churm Orcid Logo, Gareth Dunseath Orcid Logo, Charlotte Jones, Lia Bally, Christos T Nakas, Rachel Deere, Max Eckstein, Steve Bain Orcid Logo, Othmar Moser, Richard Bracken Orcid Logo

BMJ Open Diabetes Research & Care, Volume: 8, Issue: 1

Swansea University Authors: Olivia McCarthy, Jason Pitt, Rachel Churm Orcid Logo, Gareth Dunseath Orcid Logo, Charlotte Jones, Rachel Deere, Max Eckstein, Steve Bain Orcid Logo, Richard Bracken Orcid Logo

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DOI (Published version): 10.1136/bmjdrc-2020-001577

Abstract

Introduction This study sought to compare the metabolomic, hormonal and physiological responses to hypoglycemia versus euglycemia during exercise in adults with type 1 diabetes (T1D).Research design and methods Thirteen individuals with T1D (hemoglobin; 7.0%±1.3% (52.6±13.9 mmol/mol), age; 36±15 yea...

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Published in: BMJ Open Diabetes Research & Care
ISSN: 2052-4897 2052-4897
Published: 2020
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Retrospectively identified exercise sessions that ended in hypoglycemia ((HypoEx) blood glucose (BG)&#x2264;3.9 mmol/L) were compared against a participant-matched euglycemic condition ((EuEx) BG&#x2265;4.0, BG&#x2264;10.0 mmol/L). Samples were compared for detailed physiological and hormonal parameters as well as metabolically profiled via large scale targeted ultra-high-performance liquid chromatography coupled to tandem mass spectrometry. Data were assessed using univariate and multivariate analysis techniques with false discovery rate adjustment. Significant results were considered at p&#x2264;0.05.Results Cardiorespiratory and counterregulatory hormone responses, whole-body fuel use and perception of fatigue during exercise were similar under conditions of hypoglycemia and euglycemia (BG 3.5&#xB1;0.3 vs 5.8&#xB1;1.1 mmol/L, respectively p&lt;0.001). HypoEx was associated with greater adenosine salvage pathway activity (5&#x2019;-methylthioadenosine, p=0.023 and higher cysteine and methionine metabolism), increased utilization of glucogenic amino acids (glutamine, p=0.021, alanine, aspartate and glutamate metabolism and homoserine/threonine, p=0.045) and evidence of enhanced &#x3B2;-oxidation (lower carnitine p&lt;0.001, higher long-chain acylcarnitines).Conclusions Exposure to acute hypoglycemia during exercise potentiates alterations in subclinical indices of metabolic stress at the level of the metabolome. However, the physiological responses induced by dynamic physical exercise may mask the symptomatic recognition of mild hypoglycemia during exercise in people with T1D, a potential clinical safety concern that reinforces the need for diligent glucose management.</abstract><type>Journal Article</type><journal>BMJ Open Diabetes Research &amp; Care</journal><volume>8</volume><journalNumber>1</journalNumber><paginationStart/><paginationEnd/><publisher/><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint>2052-4897</issnPrint><issnElectronic>2052-4897</issnElectronic><keywords/><publishedDay>5</publishedDay><publishedMonth>10</publishedMonth><publishedYear>2020</publishedYear><publishedDate>2020-10-05</publishedDate><doi>10.1136/bmjdrc-2020-001577</doi><url/><notes/><college>COLLEGE NANME</college><department>Sport and Exercise Sciences</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>STSC</DepartmentCode><institution>Swansea University</institution><apcterm/><lastEdited>2021-01-14T13:51:36.6688350</lastEdited><Created>2020-10-06T10:54:43.6001425</Created><path><level id="1">Faculty of Science and Engineering</level><level id="2">School of Aerospace, Civil, Electrical, General and Mechanical Engineering - Sport and Exercise Sciences</level></path><authors><author><firstname>Olivia</firstname><surname>McCarthy</surname><order>1</order></author><author><firstname>Jason</firstname><surname>Pitt</surname><order>2</order></author><author><firstname>Rachel</firstname><surname>Churm</surname><orcid>0000-0001-9855-6282</orcid><order>3</order></author><author><firstname>Gareth</firstname><surname>Dunseath</surname><orcid>0000-0001-6022-862X</orcid><order>4</order></author><author><firstname>Charlotte</firstname><surname>Jones</surname><orcid/><order>5</order></author><author><firstname>Lia</firstname><surname>Bally</surname><order>6</order></author><author><firstname>Christos T</firstname><surname>Nakas</surname><order>7</order></author><author><firstname>Rachel</firstname><surname>Deere</surname><order>8</order></author><author><firstname>Max</firstname><surname>Eckstein</surname><order>9</order></author><author><firstname>Steve</firstname><surname>Bain</surname><orcid>0000-0001-8519-4964</orcid><order>10</order></author><author><firstname>Othmar</firstname><surname>Moser</surname><order>11</order></author><author><firstname>Richard</firstname><surname>Bracken</surname><orcid>0000-0002-6986-6449</orcid><order>12</order></author></authors><documents><document><filename>55338__18371__594f837882f94954b84ca36c294dc10d.pdf</filename><originalFilename>55338.pdf</originalFilename><uploaded>2020-10-08T10:04:35.0379454</uploaded><type>Output</type><contentLength>1319480</contentLength><contentType>application/pdf</contentType><version>Version of Record</version><cronfaStatus>true</cronfaStatus><documentNotes>&#xA9; Author(s) (or their employer(s)) 2020. 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spelling 2021-01-14T13:51:36.6688350 v2 55338 2020-10-06 Metabolomic, hormonal and physiological responses to hypoglycemia versus euglycemia during exercise in adults with type 1 diabetes 4fea3e19b39712dea1d051d317614572 Olivia McCarthy Olivia McCarthy true false 0103027605e3ccd2909f4170d9d2c96f Jason Pitt Jason Pitt true false c6cd8267ff0b13f2ea333bbfefdae144 0000-0001-9855-6282 Rachel Churm Rachel Churm true false fccbba9edcaee08a839a3c5cff8cbe19 0000-0001-6022-862X Gareth Dunseath Gareth Dunseath true false 62c0a30f1ea54b14a13b4ef9dcafaabd Charlotte Jones Charlotte Jones true false 3fd2ee8d0217f8487c472f52ba7c6b0a Rachel Deere Rachel Deere true false 88e3800018f862425765f3e36da8de30 Max Eckstein Max Eckstein true false 5399f4c6e6a70f3608a084ddb938511a 0000-0001-8519-4964 Steve Bain Steve Bain true false f5da81cd18adfdedb2ccb845bddc12f7 0000-0002-6986-6449 Richard Bracken Richard Bracken true false 2020-10-06 STSC Introduction This study sought to compare the metabolomic, hormonal and physiological responses to hypoglycemia versus euglycemia during exercise in adults with type 1 diabetes (T1D).Research design and methods Thirteen individuals with T1D (hemoglobin; 7.0%±1.3% (52.6±13.9 mmol/mol), age; 36±15 years, duration diabetes; 15±12 years) performed a maximum of 45 min submaximal exercise (60%±6% V̇O2max). Retrospectively identified exercise sessions that ended in hypoglycemia ((HypoEx) blood glucose (BG)≤3.9 mmol/L) were compared against a participant-matched euglycemic condition ((EuEx) BG≥4.0, BG≤10.0 mmol/L). Samples were compared for detailed physiological and hormonal parameters as well as metabolically profiled via large scale targeted ultra-high-performance liquid chromatography coupled to tandem mass spectrometry. Data were assessed using univariate and multivariate analysis techniques with false discovery rate adjustment. Significant results were considered at p≤0.05.Results Cardiorespiratory and counterregulatory hormone responses, whole-body fuel use and perception of fatigue during exercise were similar under conditions of hypoglycemia and euglycemia (BG 3.5±0.3 vs 5.8±1.1 mmol/L, respectively p<0.001). HypoEx was associated with greater adenosine salvage pathway activity (5’-methylthioadenosine, p=0.023 and higher cysteine and methionine metabolism), increased utilization of glucogenic amino acids (glutamine, p=0.021, alanine, aspartate and glutamate metabolism and homoserine/threonine, p=0.045) and evidence of enhanced β-oxidation (lower carnitine p<0.001, higher long-chain acylcarnitines).Conclusions Exposure to acute hypoglycemia during exercise potentiates alterations in subclinical indices of metabolic stress at the level of the metabolome. However, the physiological responses induced by dynamic physical exercise may mask the symptomatic recognition of mild hypoglycemia during exercise in people with T1D, a potential clinical safety concern that reinforces the need for diligent glucose management. Journal Article BMJ Open Diabetes Research & Care 8 1 2052-4897 2052-4897 5 10 2020 2020-10-05 10.1136/bmjdrc-2020-001577 COLLEGE NANME Sport and Exercise Sciences COLLEGE CODE STSC Swansea University 2021-01-14T13:51:36.6688350 2020-10-06T10:54:43.6001425 Faculty of Science and Engineering School of Aerospace, Civil, Electrical, General and Mechanical Engineering - Sport and Exercise Sciences Olivia McCarthy 1 Jason Pitt 2 Rachel Churm 0000-0001-9855-6282 3 Gareth Dunseath 0000-0001-6022-862X 4 Charlotte Jones 5 Lia Bally 6 Christos T Nakas 7 Rachel Deere 8 Max Eckstein 9 Steve Bain 0000-0001-8519-4964 10 Othmar Moser 11 Richard Bracken 0000-0002-6986-6449 12 55338__18371__594f837882f94954b84ca36c294dc10d.pdf 55338.pdf 2020-10-08T10:04:35.0379454 Output 1319480 application/pdf Version of Record true © Author(s) (or their employer(s)) 2020. This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license true eng http://creativecommons.org/licenses/by-nc/4.0/
title Metabolomic, hormonal and physiological responses to hypoglycemia versus euglycemia during exercise in adults with type 1 diabetes
spellingShingle Metabolomic, hormonal and physiological responses to hypoglycemia versus euglycemia during exercise in adults with type 1 diabetes
Olivia McCarthy
Jason Pitt
Rachel Churm
Gareth Dunseath
Charlotte Jones
Rachel Deere
Max Eckstein
Steve Bain
Richard Bracken
title_short Metabolomic, hormonal and physiological responses to hypoglycemia versus euglycemia during exercise in adults with type 1 diabetes
title_full Metabolomic, hormonal and physiological responses to hypoglycemia versus euglycemia during exercise in adults with type 1 diabetes
title_fullStr Metabolomic, hormonal and physiological responses to hypoglycemia versus euglycemia during exercise in adults with type 1 diabetes
title_full_unstemmed Metabolomic, hormonal and physiological responses to hypoglycemia versus euglycemia during exercise in adults with type 1 diabetes
title_sort Metabolomic, hormonal and physiological responses to hypoglycemia versus euglycemia during exercise in adults with type 1 diabetes
author_id_str_mv 4fea3e19b39712dea1d051d317614572
0103027605e3ccd2909f4170d9d2c96f
c6cd8267ff0b13f2ea333bbfefdae144
fccbba9edcaee08a839a3c5cff8cbe19
62c0a30f1ea54b14a13b4ef9dcafaabd
3fd2ee8d0217f8487c472f52ba7c6b0a
88e3800018f862425765f3e36da8de30
5399f4c6e6a70f3608a084ddb938511a
f5da81cd18adfdedb2ccb845bddc12f7
author_id_fullname_str_mv 4fea3e19b39712dea1d051d317614572_***_Olivia McCarthy
0103027605e3ccd2909f4170d9d2c96f_***_Jason Pitt
c6cd8267ff0b13f2ea333bbfefdae144_***_Rachel Churm
fccbba9edcaee08a839a3c5cff8cbe19_***_Gareth Dunseath
62c0a30f1ea54b14a13b4ef9dcafaabd_***_Charlotte Jones
3fd2ee8d0217f8487c472f52ba7c6b0a_***_Rachel Deere
88e3800018f862425765f3e36da8de30_***_Max Eckstein
5399f4c6e6a70f3608a084ddb938511a_***_Steve Bain
f5da81cd18adfdedb2ccb845bddc12f7_***_Richard Bracken
author Olivia McCarthy
Jason Pitt
Rachel Churm
Gareth Dunseath
Charlotte Jones
Rachel Deere
Max Eckstein
Steve Bain
Richard Bracken
author2 Olivia McCarthy
Jason Pitt
Rachel Churm
Gareth Dunseath
Charlotte Jones
Lia Bally
Christos T Nakas
Rachel Deere
Max Eckstein
Steve Bain
Othmar Moser
Richard Bracken
format Journal article
container_title BMJ Open Diabetes Research & Care
container_volume 8
container_issue 1
publishDate 2020
institution Swansea University
issn 2052-4897
2052-4897
doi_str_mv 10.1136/bmjdrc-2020-001577
college_str Faculty of Science and Engineering
hierarchytype
hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Aerospace, Civil, Electrical, General and Mechanical Engineering - Sport and Exercise Sciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Aerospace, Civil, Electrical, General and Mechanical Engineering - Sport and Exercise Sciences
document_store_str 1
active_str 0
description Introduction This study sought to compare the metabolomic, hormonal and physiological responses to hypoglycemia versus euglycemia during exercise in adults with type 1 diabetes (T1D).Research design and methods Thirteen individuals with T1D (hemoglobin; 7.0%±1.3% (52.6±13.9 mmol/mol), age; 36±15 years, duration diabetes; 15±12 years) performed a maximum of 45 min submaximal exercise (60%±6% V̇O2max). Retrospectively identified exercise sessions that ended in hypoglycemia ((HypoEx) blood glucose (BG)≤3.9 mmol/L) were compared against a participant-matched euglycemic condition ((EuEx) BG≥4.0, BG≤10.0 mmol/L). Samples were compared for detailed physiological and hormonal parameters as well as metabolically profiled via large scale targeted ultra-high-performance liquid chromatography coupled to tandem mass spectrometry. Data were assessed using univariate and multivariate analysis techniques with false discovery rate adjustment. Significant results were considered at p≤0.05.Results Cardiorespiratory and counterregulatory hormone responses, whole-body fuel use and perception of fatigue during exercise were similar under conditions of hypoglycemia and euglycemia (BG 3.5±0.3 vs 5.8±1.1 mmol/L, respectively p<0.001). HypoEx was associated with greater adenosine salvage pathway activity (5’-methylthioadenosine, p=0.023 and higher cysteine and methionine metabolism), increased utilization of glucogenic amino acids (glutamine, p=0.021, alanine, aspartate and glutamate metabolism and homoserine/threonine, p=0.045) and evidence of enhanced β-oxidation (lower carnitine p<0.001, higher long-chain acylcarnitines).Conclusions Exposure to acute hypoglycemia during exercise potentiates alterations in subclinical indices of metabolic stress at the level of the metabolome. However, the physiological responses induced by dynamic physical exercise may mask the symptomatic recognition of mild hypoglycemia during exercise in people with T1D, a potential clinical safety concern that reinforces the need for diligent glucose management.
published_date 2020-10-05T04:09:28Z
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score 11.013171

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