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Heart rate recovery after maximal exercise is impaired in healthy young adults born preterm

  • Kristin Haraldsdottir
  • Andrew M. WatsonEmail author
  • Arij G. Beshish
  • Dave F. Pegelow
  • Mari Palta
  • Laura H. Tetri
  • Melissa D. Brix
  • Ryan M. Centanni
  • Kara N. Goss
  • Marlowe W. Eldridge
Original Article

Abstract

Purpose

The long-term implications of premature birth on autonomic nervous system (ANS) function are unclear. Heart rate recovery (HRR) following maximal exercise is a simple tool to evaluate ANS function and is a strong predictor of cardiovascular disease. Our objective was to determine whether HRR is impaired in young adults born preterm (PYA).

Methods

Individuals born between 1989 and 1991 were recruited from the Newborn Lung Project, a prospectively followed cohort of subjects born preterm weighing < 1500 g with an average gestational age of 28 weeks. Age-matched term-born controls were recruited from the local population. HRR was measured for 2 min following maximal exercise testing on an upright cycle ergometer in normoxia and hypoxia, and maximal aerobic capacity (VO2max) was measured.

Results

Preterms had lower VO2max than controls (34.88 ± 5.24 v 46.15 ± 10.21 ml/kg/min, respectively, p < 0.05), and exhibited slower HRR compared to controls after 1 and 2 min of recovery in normoxia (absolute drop of 20 ± 4 v 31 ± 10 and 41 ± 7 v 54 ± 11 beats per minute (bpm), respectively, p < 0.01) and hypoxia (19 ± 5 v 26 ± 8 and 39 ± 7 v 49 ± 13 bpm, respectively, p < 0.05). After adjusting for VO2max, HRR remained slower in preterms at 1 and 2 min of recovery in normoxia (21 ± 2 v 30 ± 2 and 42 ± 3 v 52 ± 3 bpm, respectively, p < 0.05), but not hypoxia (19 ± 3 v 25 ± 2 and 40 ± 4 v 47 ± 3 bpm, respectively, p > 0.05).

Conclusions

Autonomic dysfunction as seen in this study has been associated with increased rates of cardiovascular disease in non-preterm populations, suggesting further study of the mechanisms of autonomic dysfunction after preterm birth.

Keywords

Preterm birth Autonomic function Heart rate recovery Cardiovascular disease Autonomic dysfunction Prematurity Premature birth Exercise testing Maximal aerobic capacity 

Abbreviations

ANS

Autonomic nervous system

GPAQ

Global Physical Activity Questionnaire

HR

Heart rate

HRmax

Maximal heart rate

HRR

Heart rate recovery

MET

Metabolic equivalent

Pmax

Maximal power

Tmax

Maximal time to exhaustion

VO2max

Maximal aerobic capacity

VTVO2

Oxygen consumption per kg of body weight at ventilatory threshold

Notes

Author contributions

KH, AMW, KNG, and MWE conceptualized and designed the study and are the guarantor of the content of the manuscript, including the data and analysis. KH, AMW, KNG, AGB, DFP, LHT, MDB, RMC, and MWE assisted with data collection. KH, AMW, KNG, AGB, MP, LHT, MDB, RMC, and MWE contributed to the analysis and interpretation of data. AMW conducted statistical analysis. KH and AMW prepared figures. KH drafted the initial manuscript. All authors reviewed, revised, and approved the final manuscript as submitted.

Funding

National Institutes of Health: NIH-NHLBI R01-HL115061, NIH-NHLBI R01Supplement-HL1150613 (PI Eldridge), T32-HL 07936 (Haraldsdottir).

References

  1. Amann M, Kayser B (2009) Nervous system function during exercise in hypoxia. High Alt Med Biol 10(2):149–164.  https://doi.org/10.1089/ham.2008.1105 CrossRefGoogle Scholar
  2. Amann M, Pegelow DF, Jacques AJ, Dempsey JA (2007) Inspiratory muscle work in acute hypoxia influences locomotor muscle fatigue and exercise performance of healthy humans. Am J Physiol Regul Integr Comp Physiol 293(5):R2036–R2045.  https://doi.org/10.1152/ajpregu.00442.2007 CrossRefGoogle Scholar
  3. Bates ML, Farrell ET, Eldridge MW (2014) Abnormal ventilatory responses in adults born prematurely. N Engl J Med 370(6):584–585.  https://doi.org/10.1056/NEJMc1311092 CrossRefGoogle Scholar
  4. Bilsel T, Terzi S, Akbulut T, Sayar N, Hobikoglu G, Yesilcimen K (2006) Abnormal heart rate recovery immediately after cardiopulmonary exercise testing in heart failure patients. Int Heart J 47(3):431–440.  https://doi.org/10.1536/ihj.47.431 CrossRefGoogle Scholar
  5. Bull FC, Maslin TS, Armstrong T (2009) Global physical activity questionnaire (GPAQ): nine country reliability and validity study. J Phys Activity Health 6(6):790–804CrossRefGoogle Scholar
  6. Centers for Disease Control and Prevention (2015) Preterm Birth. https://www.cdc.gov/reproductivehealth/maternalinfanthealth/pretermbirth.htm. Accessed 21 June 2017
  7. Cleland CL, Hunter RF, Kee F, Cupples ME, Sallis JF, Tully MA (2014) Validity of the global physical activity questionnaire (GPAQ) in assessing levels and change in moderate-vigorous physical activity and sedentary behaviour. BMC Public Health.  https://doi.org/10.1186/1471-2458-14-1255 Google Scholar
  8. Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. L. Erlbaum Associates, HillsdaleGoogle Scholar
  9. Cole CR, Blackstone EH, Pashkow FJ, Snader CE, Lauer MS (1999) Heart-rate recovery immediately after exercise as a predictor of mortality. N Engl J Med 341(18):1351–1357.  https://doi.org/10.1056/nejm199910283411804 CrossRefGoogle Scholar
  10. Cole CR, Foody JM, Blackstone EH, Lauer MS (2000) Heart rate recovery after submaximal exercise testing as a predictor of mortality in a cardiovascularly healthy cohort. Ann Intern Med 132(7):552–555CrossRefGoogle Scholar
  11. Davrath LR, Akselrod S, Pinhas I, Toledo E, Beck A, Elian D, Scheinowitz M (2006) Evaluation of autonomic function underlying slow postexercise heart rate recovery. Med Sci Sports Exerc 38(12):2095–2101.  https://doi.org/10.1249/01.mss.0000235360.24308.c7 CrossRefGoogle Scholar
  12. de Meautsart CC, Dyson RM, Latter JL, Berry MJ, Clifton VL, Wright IMR (2016) Influence of sympathetic activity in the control of peripheral microvascular tone in preterm infants. Pediatr Res 80(6):793–799.  https://doi.org/10.1038/pr.2016.160 CrossRefGoogle Scholar
  13. Duke JW, Elliott JE, Laurie SS, Beasley KM, Mangum TS, Hawn JA, Gladstone IM, Lovering AT (2014) Pulmonary gas exchange efficiency during exercise breathing normoxic and hypoxic gas in adults born very preterm with low diffusion capacity. J Appl Physiol (1985).  https://doi.org/10.1152/japplphysiol.00307.2014 Google Scholar
  14. Evrengul H, Tanriverdi H, Kose S, Amasyali B, Kilic A, Celik T, Turhan H (2006) The relationship between heart rate recovery and heart rate variability in coronary artery disease. Ann Noninvasive Electrocardiol 11(2):154–162.  https://doi.org/10.1111/j.1542-474X.2006.00097.x CrossRefGoogle Scholar
  15. Farrell ET, Bates ML, Pegelow DF, Palta M, Eickhoff JC, O’Brien MJ, Eldridge MW (2015) Pulmonary gas exchange and exercise capacity in adults born preterm. Ann Am Thorac Soc 12(8):1130–1137.  https://doi.org/10.1513/AnnalsATS.201410-470OC Google Scholar
  16. Florea VG, Cohn JN (2014) The autonomic nervous system and heart failure. Circ Res 114(11):1815–1826.  https://doi.org/10.1161/circresaha.114.302589 CrossRefGoogle Scholar
  17. Gagnon R, Campbell K, Hunse C, Patrick J (1987) Patterns of human-fetal heart-rate accelerations from 26 weeks to term. Am J Obstet Gynecol 157(3):743–748CrossRefGoogle Scholar
  18. Haraldsdottir K, Watson AM, Goss KN, Beshish AG, Pegelow DF, Palta M, Tetri LH, Barton GP, Brix MD, Centanni RM, Eldridge MW (2018) Impaired autonomic function in adolescents born preterm. Physiol Rep 6(6):e13620.  https://doi.org/10.14814/phy2.13620 CrossRefGoogle Scholar
  19. Hargens TA, Guill SG, Zedalis D, Gregg JM, Nickols-Richardson SM, Herbert WG (2008) Attenuated heart rate recovery following exercise testing in overweight young men with untreated obstructive sleep apnea. Sleep 31(1):104–110CrossRefGoogle Scholar
  20. Hautala AJ, Rankinen T, Kiviniemi AM, Makikallio TH, Huikuri HV, Bouchard C, Tulppo MP (2006) Heart rate recovery after maximal exercise is associated with acetylcholine receptor M2 (CHRM2) gene polymorphism. Am J Physiol Heart Circ Physiol 291(1):H459–H466.  https://doi.org/10.1152/ajpheart.01193.2005 CrossRefGoogle Scholar
  21. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6(2):65–70Google Scholar
  22. Imai K, Sato H, Hori M, Kusuoka H, Ozaki H, Yokoyama H, Takeda H, Inoue M, Kamada T (1994) Vagally mediated heart-rate recovery after exercise is accelerated in athletes but blunted in patients with chronic heart-failure. J Am Coll Cardiol 24(6):1529–1535CrossRefGoogle Scholar
  23. Jae SY, Carnethon MR, Heffernan KS, Choi YH, Lee MK, Park WH, Fernhall B (2008) Slow heart rate recovery after exercise is associated with carotid atherosclerosis. Atherosclerosis 196(1):256–261.  https://doi.org/10.1016/j.atherosclerosis.2006.10.023 CrossRefGoogle Scholar
  24. Johansson S, Norman M, Legnevall L, Dalmaz Y, Lagercrantz H, Vanpee M (2007) Increased catecholamines and heart rate in children with low birth weight: perinatal contributions to sympathoadrenal overactivity. J Intern Med 261(5):480–487.  https://doi.org/10.1111/j.1365-2796.2007.01776.x CrossRefGoogle Scholar
  25. Joyner MJ, Charkoudian N, Wallin BG (2010) Sympathetic nervous system and blood pressure in humans: individualized patterns of regulation and their implications. Hypertension 56(1):10–16.  https://doi.org/10.1161/HYPERTENSIONAHA.109.140186 CrossRefGoogle Scholar
  26. Kennedy MD, Warburton DE, Boliek CA, Esch BT, Scott JM, Haykowsky MJ (2008) The oxygen delivery response to acute hypoxia during incremental knee extension exercise differs in active and trained males. Dyn Med DM 7:11.  https://doi.org/10.1186/1476-5918-7-11 CrossRefGoogle Scholar
  27. Kishi T (2012) Heart failure as an autonomic nervous system dysfunction. J Cardiol 59(2):117–122.  https://doi.org/10.1016/j.jjcc.2011.12.006 CrossRefGoogle Scholar
  28. Kleiger RE, Stein PK, Bigger JT (2005) Heart rate variability: Measurement and clinical utility. Ann Noninvasive Electrocardiol 10(1):88–101.  https://doi.org/10.1111/j.1542-474X.2005.10101.x CrossRefGoogle Scholar
  29. Kuo HK, Gore JM (2015) Relation of heart rate recovery after exercise to insulin resistance and chronic inflammation in otherwise healthy adolescents and adults: results from the National Health and Nutrition Examination Survey (NHANES) 1999–2004. Clin Res Cardiol 104(9):764–772.  https://doi.org/10.1007/s00392-015-0843-2 CrossRefGoogle Scholar
  30. Lewandowski AJ, Bradlow WM, Augustine D, Davis EF, Francis J, Singhal A, Lucas A, Neubauer S, McCormick K, Leeson P (2013) Right ventricular systolic dysfunction in young adults born preterm. Circulation 128(7):713–720.  https://doi.org/10.1161/circulationaha.113.002583 CrossRefGoogle Scholar
  31. Mathewson KJ, Van Lieshout RJ, Saigal S, Morrison KM, Boyle MH, Schmidt LA (2015) Autonomic functioning in young adults born at extremely low birth weight. Glob Pediatr Health 2:2333794 × 15589560.  https://doi.org/10.1177/2333794X15589560 Google Scholar
  32. Midgley AW, McNaughton LR, Polman R, Marchant D (2007) Criteria for determination of maximal oxygen uptake—a brief critique and recommendations for future research. Sports Med 37(12):1019–1028.  https://doi.org/10.2165/00007256-200737120-00002 CrossRefGoogle Scholar
  33. Minai OA, Gudavalli R, Mummadi S, Liu XB, McCarthy K, Dweik RA (2012) Heart rate recovery predicts clinical worsening in patients with pulmonary arterial hypertension. Am J Respir Crit Care Med 185(4):400–408.  https://doi.org/10.1164/rccm.201105-0848OC CrossRefGoogle Scholar
  34. Mitchell JH (1985) Cardiovascular control during exercise-central and reflex neural mechanisms. Am J Cardiol 55(10):D34–D41.  https://doi.org/10.1016/0002-9149(85)91053-7 CrossRefGoogle Scholar
  35. Morshedi-Meibodi A, Larson MG, Levy D, O’Donnell CJ, Vasan RS (2002) Heart rate recovery after treadmill exercise testing and risk of cardiovascular disease events (the Framingham Heart Study). Am J Cardiol 90(8):848–852.  https://doi.org/10.1016/s0002-9149(02)02706-6 CrossRefGoogle Scholar
  36. Norman M (2010) Preterm birth—an emerging risk factor for adult hypertension? Semin Perinatol 34(3):183–187.  https://doi.org/10.1053/j.sempen.2010.02.009 CrossRefGoogle Scholar
  37. Ostojic SM, Markovic G, Calleja-Gonzalez J, Jakovljevic DG, Vucetic V, Stojanovic MD (2010) Ultra short-term heart rate recovery after maximal exercise in continuous versus intermittent endurance athletes. Eur J Appl Physiol 108(5):1055–1059.  https://doi.org/10.1007/s00421-009-1313-1 CrossRefGoogle Scholar
  38. Palta M, Weinstein MR, McGuinness G, Gabbert D, Brady W, Peters ME (1994) A population study. Mortality and morbidity after availability of surfactant therapy. Newborn Lung Project Arch Pediatr Adolesc Med 148(12):1295–1301CrossRefGoogle Scholar
  39. Palta M, Sadek M, Barnet JH, Evans M, Weinstein MR, McGuinness G, Peters ME, Gabbert D, Fryback D, Farrell P (1998) Evaluation of criteria for chronic lung disease in surviving very low birth weight infants. Newborn Lung Project J Pediatr 132(1):57–63Google Scholar
  40. Palta M, Sadek-Badawi M, Evans M, Weinstein MR, McGuinnes G (2000) Functional assessment of a multicenter very low-birth-weight cohort at age 5 years. Newborn Lung Project. Arch Pediatr Adolesc Med 154(1):23–30Google Scholar
  41. Palta M, Sadek-Badawi M, Sheehy M, Albanese A, Weinstein M, McGuinness G, Peters ME (2001) Respiratory symptoms at age 8 years in a cohort of very low birth weight children. Am J Epidemiol 154(6):521–529CrossRefGoogle Scholar
  42. Patural H, Barthelemy JC, Pichot V, Mazzocchi C, Teyssier G, Damon G, Roche F (2004) Birth prematurity determines prolonged autonomic nervous system immaturity. Clin Auton Res 14(6):391–395.  https://doi.org/10.1007/s10286-004-0216-9 CrossRefGoogle Scholar
  43. Peacock JL, Marston L, Marlow N, Calvert SA, Greenough A (2012) Neonatal and infant outcome in boys and girls born very prematurely. Pediatr Res 71(3):305–310.  https://doi.org/10.1038/pr.2011.50 CrossRefGoogle Scholar
  44. Pierpont GL, Adabag S, Yannopoulos D (2013) Pathophysiology of exercise heart rate recovery: a comprehensive analysis. Ann Noninvasive Electrocardiol 18(2):107–117.  https://doi.org/10.1111/anec.12061 CrossRefGoogle Scholar
  45. Porges SW, Furman SA (2011) The early development of the autonomic nervous system provides a neural platform for social behaviour: a polyvagal perspective. Infant Child Dev 20(1):106–118.  https://doi.org/10.1002/icd.688 CrossRefGoogle Scholar
  46. Prabhakar NR, Peng YJ (2004) Peripheral chemoreceptors in health and disease. J Appl Physiol 96(1):359–366.  https://doi.org/10.1152/japplphysiol.00809.2003 CrossRefGoogle Scholar
  47. Qiu SH, Cai X, Sun ZL, Li L, Zuegel M, Steinacker JM, Schumann U (2017) Heart rate recovery and risk of cardiovascular events and all-cause mortality: a meta-analysis of prospective cohort studies. J Am Heart Assoc.  https://doi.org/10.1161/jaha.117.005505 Google Scholar
  48. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  49. Ramos RP, Arakaki JSO, Barbosa P, Treptow E, Valois FM, Ferreira EVM, Nery LE, Neder JA (2012) Heart rate recovery in pulmonary arterial hypertension: Relationship with exercise capacity and prognosis. Am Heart J 163(4):580–588.  https://doi.org/10.1016/j.ahj.2012.01.023 CrossRefGoogle Scholar
  50. Savin WM, Davidson DM, Haskell WL (1982) Autonomic contribution to heart-rate recovery from exercise in humans. J Appl Physiol 53(6):1572–1575CrossRefGoogle Scholar
  51. Thayer JF, Lane RD (2007) The role of vagal function in the risk for cardiovascular disease and mortality. Biol Psychol 74(2):224–242.  https://doi.org/10.1016/j.biopsycho.2005.11.013 CrossRefGoogle Scholar
  52. Watanabe J, Thamilarasan M, Blackstone EH, Thomas JD, Lauer MS (2001) Heart rate recovery immediately after treadmill exercise and left ventricular systolic dysfunction as predictors of mortality—the case of stress echocardiography. Circulation 104(16):1911–1916CrossRefGoogle Scholar
  53. Watson AM, Brickson SL, Prawda ER, Sanfilippo JL (2017) Short-term heart rate recovery is related to aerobic fitness in elite intermittent sport athletes. J Strength Conditioning Res 31(4):1055–1061.  https://doi.org/10.1519/jsc.0000000000001567 CrossRefGoogle Scholar
  54. Weinstein MR, Peters ME, Sadek M, Palta M (1994) A new radiographic scoring system for bronchopulmonary dysplasia. Newborn Lung Project Pediatr Pulmonol 18(5):284–289CrossRefGoogle Scholar
  55. Yiallourou SR, Witcombe NB, Sands SA, Walker AM, Horne RSC (2013) The development of autonomic cardiovascular control is altered by preterm birth. Early Human Dev 89(3):145–152.  https://doi.org/10.1016/j.earlhumdev.2012.09.009 CrossRefGoogle Scholar
  56. Yiallourou SR, Wallace EM, Whatley C, Odoi A, Hollis S, Weichard AJ, Muthusamy JS, Varma S, Cameron J, Narayan O, Horne RSC (2017) Sleep: a window into autonomic control in children born preterm and growth restricted. Sleep.  https://doi.org/10.1093/sleep/zsx048 Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Kristin Haraldsdottir
    • 1
    • 5
    return OK on get
  • Andrew M. Watson
    • 2
    Email author
  • Arij G. Beshish
    • 1
  • Dave F. Pegelow
    • 1
  • Mari Palta
    • 4
  • Laura H. Tetri
    • 1
  • Melissa D. Brix
    • 1
  • Ryan M. Centanni
    • 1
  • Kara N. Goss
    • 1
    • 3
  • Marlowe W. Eldridge
    • 1
  1. 1.Department of PediatricsUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.Department of Orthopedics and RehabilitationUniversity of Wisconsin-MadisonMadisonUSA
  3. 3.Department of MedicineUniversity of Wisconsin-MadisonMadisonUSA
  4. 4.Department of Biostatistics and Medical InformaticsUniversity of Wisconsin-MadisonMadisonUSA
  5. 5.Department of KinesiologyUniversity of Wisconsin-MadisonMadisonUSA

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