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Published in: Journal of Cardiovascular Magnetic Resonance 1/2020

Open Access 01-12-2020 | Dyspnea | Research

Evaluation of dyspnea of unknown etiology in HIV patients with cardiopulmonary exercise testing and cardiovascular magnetic resonance imaging

Authors: Andrew J. Patterson, Anuja Sarode, Sadeer Al-Kindi, Lauren Shaver, Rahul Thomas, Evelyn Watson, Mohamad Amer Alaiti, Yuchi Liu, Jessie Hamilton, Nicole Seiberlich, Imran Rashid, Robert Gilkeson, Robert Schilz, Brian Hoit, Trevor Jenkins, Melissa Zullo, Eduardo Bossone, Christopher Longenecker, Orlando Simonetti, Sanjay Rajagopalan

Published in: Journal of Cardiovascular Magnetic Resonance | Issue 1/2020

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Abstract

Aim

Human Immunodeficiency Virus (HIV) patients commonly experience dyspnea for which an immediate cause may not be always apparent. In this prospective cohort study of HIV patients with exercise limitation, we use cardiopulmonary exercise testing (CPET) coupled with exercise cardiovascular magnetic resonance (CMR) to elucidate etiologies of dyspnea.

Methods and results

Thirty-four HIV patients on antiretroviral therapy with dyspnea and exercise limitation (49.7 years, 65% male, mean absolute CD4 count 700) underwent comprehensive evaluation with combined rest and maximal exercise treadmill CMR and CPET. The overall mean oxygen consumption (VO2) peak was reduced at 23.2 ± 6.9 ml/kg/min with 20 patients (58.8% of overall cohort) achieving a respiratory exchange ratio > 1. The ventilatory efficiency (VE)/VCO2 slope was elevated at 36 ± 7.92, while ventilatory reserve (VE: maximal voluntary ventilation (MVV)) was within normal limits. The mean absolute right ventricular (RV) and left ventricular (LV) contractile reserves were preserved at 9.0% ± 11.2 and 9.4% ± 9.4, respectively. The average resting and post-exercise mean average pulmonary artery velocities were 12.2 ± 3.9 cm/s and 18.9 ± 8.3 respectively, which suggested lack of exercise induced pulmonary artery hypertension (PAH). LV but not RV delayed enhancement were identified in five patients. Correlation analysis found no relationship between peak VO2 measures of contractile RV or LV reserve, but LV and RV stroke volume correlated with PET CO2 (p = 0.02, p = 0.03).

Conclusion

Well treated patients with HIV appear to have conserved RV and LV function, contractile reserve and no evidence of exercise induced PAH. However, we found evidence of impaired ventilation suggesting a non-cardiopulmonary etiology for dyspnea.
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Literature
1.
go back to reference Barnett CF, Hsue PY. Human immunodeficiency virus-associated pulmonary arterial hypertension. Clin Chest Med. 2013;34(2):283–92.CrossRef Barnett CF, Hsue PY. Human immunodeficiency virus-associated pulmonary arterial hypertension. Clin Chest Med. 2013;34(2):283–92.CrossRef
2.
go back to reference Pellicelli AM, Barbaro G, Palmieri F, et al. Primary pulmonary hypertension in HIV patients: a systematic review. Angiology. 2001;52(1):31–41.CrossRef Pellicelli AM, Barbaro G, Palmieri F, et al. Primary pulmonary hypertension in HIV patients: a systematic review. Angiology. 2001;52(1):31–41.CrossRef
3.
go back to reference Hsue PY, Deeks SG, Farah HH, et al. Role of HIV and human herpesvirus-8 infection in pulmonary arterial hypertension. AIDS (London, England). 2008;22(7):825–33.CrossRef Hsue PY, Deeks SG, Farah HH, et al. Role of HIV and human herpesvirus-8 infection in pulmonary arterial hypertension. AIDS (London, England). 2008;22(7):825–33.CrossRef
4.
go back to reference Waddingham PH, Bhattacharyya S, Zalen JV, Lloyd G. Contractile reserve as a predictor of prognosis in patients with non-ischaemic systolic heart failure and dilated cardiomyopathy: a systematic review and meta-analysis. Echo Res Pract. 2018;5(1):1–9.CrossRef Waddingham PH, Bhattacharyya S, Zalen JV, Lloyd G. Contractile reserve as a predictor of prognosis in patients with non-ischaemic systolic heart failure and dilated cardiomyopathy: a systematic review and meta-analysis. Echo Res Pract. 2018;5(1):1–9.CrossRef
5.
go back to reference Hsu S, Houston BA, Tampakakis E, et al. Right ventricular functional Reserve in Pulmonary Arterial Hypertension. Circulation. 2016;133(24):2413–22.CrossRef Hsu S, Houston BA, Tampakakis E, et al. Right ventricular functional Reserve in Pulmonary Arterial Hypertension. Circulation. 2016;133(24):2413–22.CrossRef
6.
go back to reference Groepenhoff H, Vonk-Noordegraaf A, van de Veerdonk MC, Boonstra A, Westerhof N, Bogaard HJ. Prognostic relevance of changes in exercise test variables in pulmonary arterial hypertension. PLoS One. 2013;8(9):1–11.CrossRef Groepenhoff H, Vonk-Noordegraaf A, van de Veerdonk MC, Boonstra A, Westerhof N, Bogaard HJ. Prognostic relevance of changes in exercise test variables in pulmonary arterial hypertension. PLoS One. 2013;8(9):1–11.CrossRef
7.
go back to reference Maron BA, Cockrill BA, Waxman AB, Systrom DM. The invasive cardiopulmonary exercise test. Circulation. 2013;127(10):1157–64.CrossRef Maron BA, Cockrill BA, Waxman AB, Systrom DM. The invasive cardiopulmonary exercise test. Circulation. 2013;127(10):1157–64.CrossRef
8.
go back to reference Naeije R, Saggar R, Badesch D, et al. Exercise-Induced Pulmonary Hypertension: Translating Pathophysiological Concepts Into Clinical Practice. Chest. 2018;154(1):10.CrossRef Naeije R, Saggar R, Badesch D, et al. Exercise-Induced Pulmonary Hypertension: Translating Pathophysiological Concepts Into Clinical Practice. Chest. 2018;154(1):10.CrossRef
9.
go back to reference Foster EL, Arnold JW, Jekic M, et al. MR-compatible treadmill for exercise stress cardiac magnetic resonance imaging. Magn Reson Med. 2012;67(3):880–9.CrossRef Foster EL, Arnold JW, Jekic M, et al. MR-compatible treadmill for exercise stress cardiac magnetic resonance imaging. Magn Reson Med. 2012;67(3):880–9.CrossRef
10.
go back to reference Alaiti MA, Goud A, Ramani G, et al. Design of the exercise MRI evaluation of HIV-pulmonary arterial hypertension longitudinal determinants (EXALTED) trial. J Cardiovasc Med. 2017;18:11.CrossRef Alaiti MA, Goud A, Ramani G, et al. Design of the exercise MRI evaluation of HIV-pulmonary arterial hypertension longitudinal determinants (EXALTED) trial. J Cardiovasc Med. 2017;18:11.CrossRef
11.
go back to reference Mahler DA, Wells CK. Evaluation of clinical methods for rating dyspnea. Chest. 1988;93(3):580–6.CrossRef Mahler DA, Wells CK. Evaluation of clinical methods for rating dyspnea. Chest. 1988;93(3):580–6.CrossRef
12.
go back to reference Beaver WL, Wasserman K, Whipp BJ. A new method for detecting anaerobic threshold by gas exchange. J Appl Physiol (1985). 1986;60(6):2020–7.CrossRef Beaver WL, Wasserman K, Whipp BJ. A new method for detecting anaerobic threshold by gas exchange. J Appl Physiol (1985). 1986;60(6):2020–7.CrossRef
13.
go back to reference Barber NJ, Ako EO, Kowalik GT, et al. Magnetic Resonance-Augmented Cardiopulmonary Exercise Testing: Comprehensively Assessing Exercise Intolerance in Children With Cardiovascular Disease. Circ Cardiovasc Imaging. 2016;9:12.CrossRef Barber NJ, Ako EO, Kowalik GT, et al. Magnetic Resonance-Augmented Cardiopulmonary Exercise Testing: Comprehensively Assessing Exercise Intolerance in Children With Cardiovascular Disease. Circ Cardiovasc Imaging. 2016;9:12.CrossRef
14.
go back to reference Kramer CM, Barkhausen J, Flamm SD, Kim RJ, Nagel E. Society for Cardiovascular Magnetic Resonance Board of Trustees Task Force on Standardized P. Standardized cardiovascular magnetic resonance (CMR) protocols 2013 update. J Cardiovasc Magn Reson. 2013;15:91.CrossRef Kramer CM, Barkhausen J, Flamm SD, Kim RJ, Nagel E. Society for Cardiovascular Magnetic Resonance Board of Trustees Task Force on Standardized P. Standardized cardiovascular magnetic resonance (CMR) protocols 2013 update. J Cardiovasc Magn Reson. 2013;15:91.CrossRef
15.
go back to reference Lin HY, Bender JA, Ding Y, et al. Shared velocity encoding: a method to improve the temporal resolution of phase-contrast velocity measurements. Magn Reson Med. 2012;68(3):703–10.CrossRef Lin HY, Bender JA, Ding Y, et al. Shared velocity encoding: a method to improve the temporal resolution of phase-contrast velocity measurements. Magn Reson Med. 2012;68(3):703–10.CrossRef
16.
go back to reference Aandal G, Nadig V, Yeh V, Rajah P, Jenkins T, Sattar A, et al. Evaluation of left ventricular ejection fraction using through-time radial GRAPPA. J Cardiovasc Magn Reson. 2014;16(1):79.CrossRef Aandal G, Nadig V, Yeh V, Rajah P, Jenkins T, Sattar A, et al. Evaluation of left ventricular ejection fraction using through-time radial GRAPPA. J Cardiovasc Magn Reson. 2014;16(1):79.CrossRef
17.
go back to reference Fletcher GF, Ades PA, Kligfield P, et al. Exercise standards for testing and training: a scientific statement from the American Heart Association. Circulation. 2013;128(8):873–934.CrossRef Fletcher GF, Ades PA, Kligfield P, et al. Exercise standards for testing and training: a scientific statement from the American Heart Association. Circulation. 2013;128(8):873–934.CrossRef
18.
go back to reference Sanz J, Kuschnir P, Rius T, et al. Pulmonary arterial hypertension: noninvasive detection with phase-contrast MR imaging. Radiology. 2007;243(1):70–9.CrossRef Sanz J, Kuschnir P, Rius T, et al. Pulmonary arterial hypertension: noninvasive detection with phase-contrast MR imaging. Radiology. 2007;243(1):70–9.CrossRef
19.
go back to reference Koo TK, Li MY. A guideline of selecting and reporting Intraclass correlation coefficients for reliability research. J Chiropr Med. 2016;15(2):155–63.CrossRef Koo TK, Li MY. A guideline of selecting and reporting Intraclass correlation coefficients for reliability research. J Chiropr Med. 2016;15(2):155–63.CrossRef
20.
go back to reference Lafountain RA, da Silveira JS, Varghese J, et al. Cardiopulmonary exercise testing in the MRI environment. Physiol Meas. 2016;37(4):N11–25.CrossRef Lafountain RA, da Silveira JS, Varghese J, et al. Cardiopulmonary exercise testing in the MRI environment. Physiol Meas. 2016;37(4):N11–25.CrossRef
21.
go back to reference Webel AR, Perazzo J, Longenecker CT, et al. The influence of exercise on cardiovascular health in sedentary adults with human immunodeficiency virus. J Cardiovasc Nurs. 2018;33(3):239–47.CrossRef Webel AR, Perazzo J, Longenecker CT, et al. The influence of exercise on cardiovascular health in sedentary adults with human immunodeficiency virus. J Cardiovasc Nurs. 2018;33(3):239–47.CrossRef
22.
go back to reference Chisati EM, Vasseljen O. Aerobic endurance in HIV-positive young adults and HIV-negative controls in Malawi. Malawi Med J. 2015;27(1):5–9.CrossRef Chisati EM, Vasseljen O. Aerobic endurance in HIV-positive young adults and HIV-negative controls in Malawi. Malawi Med J. 2015;27(1):5–9.CrossRef
23.
go back to reference Kiely DG, Elliot CA, Sabroe I, Condliffe R. Pulmonary hypertension: diagnosis and management. BMJ. 2013;346:f2028.CrossRef Kiely DG, Elliot CA, Sabroe I, Condliffe R. Pulmonary hypertension: diagnosis and management. BMJ. 2013;346:f2028.CrossRef
24.
go back to reference Tolle JJ, Waxman AB, Van Horn TL, Pappagianopoulos PP, Systrom DM. Exercise-induced pulmonary arterial hypertension. Circulation. 2008;118(21):2183–9.CrossRef Tolle JJ, Waxman AB, Van Horn TL, Pappagianopoulos PP, Systrom DM. Exercise-induced pulmonary arterial hypertension. Circulation. 2008;118(21):2183–9.CrossRef
25.
go back to reference Holloway CJ, Ntusi N, Suttie J, Mahmod M, et al. Comprehensive cardiac magnetic resonance imaging and spectroscopy reveal a high burden of myocardial disease in HIV patients. Circulation. 2013;128(8):814–22.CrossRef Holloway CJ, Ntusi N, Suttie J, Mahmod M, et al. Comprehensive cardiac magnetic resonance imaging and spectroscopy reveal a high burden of myocardial disease in HIV patients. Circulation. 2013;128(8):814–22.CrossRef
26.
go back to reference Luetkens JA, Doerner J, Schwarze-Zander C, et al. Cardiac magnetic resonance reveals signs of subclinical myocardial inflammation in asymptomatic HIV-infected patients. Circ Cardiovasc Imaging. 2016;9(3):e004091.CrossRef Luetkens JA, Doerner J, Schwarze-Zander C, et al. Cardiac magnetic resonance reveals signs of subclinical myocardial inflammation in asymptomatic HIV-infected patients. Circ Cardiovasc Imaging. 2016;9(3):e004091.CrossRef
27.
go back to reference Swift AJ, Rajaram S, Capener D, et al. LGE patterns in pulmonary hypertension do not impact overall mortality. JACC Cardiovasc Imaging. 2014;7(12):1209–17.CrossRef Swift AJ, Rajaram S, Capener D, et al. LGE patterns in pulmonary hypertension do not impact overall mortality. JACC Cardiovasc Imaging. 2014;7(12):1209–17.CrossRef
28.
go back to reference Lewis GD, Shah RV, Pappagianopolas PP, Systrom DM, Semigran MJ. Determinants of ventilatory efficiency in heart failure: the role of right ventricular performance and pulmonary vascular tone. Circ Heart Fail. 2008;1(4):227–33.CrossRef Lewis GD, Shah RV, Pappagianopolas PP, Systrom DM, Semigran MJ. Determinants of ventilatory efficiency in heart failure: the role of right ventricular performance and pulmonary vascular tone. Circ Heart Fail. 2008;1(4):227–33.CrossRef
29.
go back to reference Matsumoto A, Itoh H, Eto Y, et al. End-tidal CO2 pressure decreases during exercise in cardiac patients: association with severity of heart failure and cardiac output reserve. J Am Coll Cardiol. 2000;36(1):242–9.CrossRef Matsumoto A, Itoh H, Eto Y, et al. End-tidal CO2 pressure decreases during exercise in cardiac patients: association with severity of heart failure and cardiac output reserve. J Am Coll Cardiol. 2000;36(1):242–9.CrossRef
30.
go back to reference Tanabe Y, Hosaka Y, Ito M, Ito E, Suzuki K. Significance of end-tidal P (CO(2)) response to exercise and its relation to functional capacity in patients with chronic heart failure. Chest. 2001;119(3):811–7.CrossRef Tanabe Y, Hosaka Y, Ito M, Ito E, Suzuki K. Significance of end-tidal P (CO(2)) response to exercise and its relation to functional capacity in patients with chronic heart failure. Chest. 2001;119(3):811–7.CrossRef
31.
go back to reference Cicoira M, Zanolla L, Franceschini L, et al. Skeletal muscle mass independently predicts peak oxygen consumption and ventilatory response during exercise in noncachectic patients with chronic heart failure. J Am Coll Cardiol. 2001;37(8):2080–5.CrossRef Cicoira M, Zanolla L, Franceschini L, et al. Skeletal muscle mass independently predicts peak oxygen consumption and ventilatory response during exercise in noncachectic patients with chronic heart failure. J Am Coll Cardiol. 2001;37(8):2080–5.CrossRef
32.
go back to reference Echeverria P, Bonjoch A, Puig J, et al. High prevalence of sarcopenia in HIV-infected individuals. Biomed Res Int. 2018;2018:5074923.CrossRef Echeverria P, Bonjoch A, Puig J, et al. High prevalence of sarcopenia in HIV-infected individuals. Biomed Res Int. 2018;2018:5074923.CrossRef
33.
go back to reference Webel AR, Sattar A, Funderburg NT, et al. Alcohol and dietary factors associate with gut integrity and inflammation in HIV-infected adults. HIV Med. 2017;18(6):402–11.CrossRef Webel AR, Sattar A, Funderburg NT, et al. Alcohol and dietary factors associate with gut integrity and inflammation in HIV-infected adults. HIV Med. 2017;18(6):402–11.CrossRef
34.
go back to reference Robinson-Papp J, Simpson DM. Neuromuscular diseases associated with HIV-1 infection. Muscle Nerve. 2009;40(6):1043–53.CrossRef Robinson-Papp J, Simpson DM. Neuromuscular diseases associated with HIV-1 infection. Muscle Nerve. 2009;40(6):1043–53.CrossRef
35.
go back to reference Koethe JR, Heimburger DC, PrayGod G, Filteau S. From wasting to obesity: the contribution of nutritional status to immune activation in HIV infection. J Infect Dis. 2016;214(Suppl 2):S75–82.CrossRef Koethe JR, Heimburger DC, PrayGod G, Filteau S. From wasting to obesity: the contribution of nutritional status to immune activation in HIV infection. J Infect Dis. 2016;214(Suppl 2):S75–82.CrossRef
Metadata
Title
Evaluation of dyspnea of unknown etiology in HIV patients with cardiopulmonary exercise testing and cardiovascular magnetic resonance imaging
Authors
Andrew J. Patterson
Anuja Sarode
Sadeer Al-Kindi
Lauren Shaver
Rahul Thomas
Evelyn Watson
Mohamad Amer Alaiti
Yuchi Liu
Jessie Hamilton
Nicole Seiberlich
Imran Rashid
Robert Gilkeson
Robert Schilz
Brian Hoit
Trevor Jenkins
Melissa Zullo
Eduardo Bossone
Christopher Longenecker
Orlando Simonetti
Sanjay Rajagopalan
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Journal of Cardiovascular Magnetic Resonance / Issue 1/2020
Electronic ISSN: 1532-429X
DOI
https://doi.org/10.1186/s12968-020-00664-6

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