Loss of nocturnal dipping pattern of skin sympathetic nerve activity during and following an extended-duration work shift in residents in training

      Highlights

      • Skin sympathetic nerve activity (SKNA) reflects cardiac sympathetic tone.
      • Noninvasive neuro-electrocardiography (neuECG) can be used to investigate SKNA.
      • SKNA presents a dip night in healthy young adults.
      • The SKNA dip is impaired by working a nightshift, with a delayed recovery.
      • The neuECG serves as a useful tool to detect subclinical autonomic disturbances.

      Abstract

      Background

      Extended-duration work shifts (EDWSs) might affect the health of physician residents, causing autonomic alteration. Skin sympathetic nerve activity (SKNA) recorded by noninvasive neuro-electrocardiography (neuECG) is used to estimate cardiac sympathetic tone. In this study, we aim to evaluate the impact of EDWSs on nocturnal SKNA assessed in resident doctors.

      Methods

      Twenty-four residents working EDWSs and 12 PhD students not working nightshift schedules were prospectively recruited. The neuECG was performed between 12 am and 6 am for 5 consecutive nights. SKNA was filtered from neuECG recorded signals. The questionnaires regarding work stress and sleep quality, blood pressure, and salivary alpha-amylase and cortisol levels were administered.

      Results

      The hours of weekly working and sleep opportunities were similar between residents and students, while residents reported more work stress and worse sleep quality. In residents, SKNA at 6 am (SKNA6am) was significantly higher than SKNA2am during the precall night, revealing a dipping pattern. However, the SKNA dipping disappeared during the on-call night and prominently flattened during the first postcall night, the full recovery of which was delayed until the second postcall nights. The morning blood pressure and salivary alpha-amylase and cortisol levels were similar between the precall and postcall days. In contrast, SKNA in students exhibited a constant dipping profile for all recorded nights.

      Conclusions

      In healthy young adults, SKNA presents a dip night. The SKNA dip is impaired by working a nightshift, with a delayed recovery. The neuECG might serve as a useful tool to detect subclinical autonomic disturbances in shiftworkers.

      Graphical abstract

      Keywords

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      References

        • Landrigan C.P.
        • Rothschild J.M.
        • Cronin J.W.
        • Kaushal R.
        • Burdick E.
        • Katz J.T.
        • et al.
        Effect of reducing interns' work hours on serious medical errors in intensive care units.
        N Engl J Med. 2004; 351: 1838-1848
        • Basner M.
        • Dinges D.F.
        • Shea J.A.
        • Small D.S.
        • Zhu J.
        • Norton L.
        • et al.
        Sleep and alertness in medical interns and residents: an observational study on the role of extended shifts.
        Sleep. 2017; 40: 027
        • Barger L.K.
        • Sullivan J.P.
        • Blackwell T.
        • O'Brien C.S.
        • St Hilaire M.A.
        • Rahman S.A.
        • et al.
        Effects on resident work hours, sleep duration, and work experience in a randomized order safety trial evaluating resident-physician schedules (ROSTERS).
        Sleep. 2019; 42: 110
        • Takase B.
        • Akima T.
        • Satomura K.
        • Ohsuzu F.
        • Mastui T.
        • Ishihara M.
        • et al.
        Effects of chronic sleep deprivation on autonomic activity by examining heart rate variability, plasma catecholamine, and intracellular magnesium levels.
        Biomed Pharmacother. 2004; 58: S35-S39
        • Hulsegge G.
        • Gupta N.
        • Proper K.I.
        • van Lobenstein N.
        • IJzelenberg W.
        • Hallman D.M.
        • et al.
        Shift work is associated with reduced heart rate variability among men but not women.
        Int J Cardiol. 2018; 258: 109-114
        • Kusayama T.
        • Wong J.
        • Liu X.
        • He W.
        • Doytchinova A.
        • Robinson E.A.
        • et al.
        Simultaneous noninvasive recording of electrocardiogram and skin sympathetic nerve activity (neuECG).
        Nat Protoc. 2020; 15: 1853-1877
        • Taniguchi T.
        • Morimoto M.
        • Taniguchi Y.
        • Takasaka M.
        • Totoki T.
        Cutaneous distribution of sympathetic postganglionic fibers from stellate ganglion: A retrograde axonal tracing study using wheat germ agglutinin conjugated with horseradish peroxidase.
        J Anesth. 1994; 8: 441-449
        • Chan Y.H.
        • Tsai W.C.
        • Shen C.
        • Han S.
        • Chen L.S.
        • Lin S.F.
        • et al.
        Subcutaneous nerve activity is more accurate than heart rate variability in estimating cardiac sympathetic tone in ambulatory dogs with myocardial infarction.
        Heart Rhythm. 2015; 12: 1619-1627
        • Jiang Z.
        • Zhao Y.
        • Doytchinova A.
        • Kamp N.J.
        • Tsai W.C.
        • Yuan Y.
        • et al.
        Using skin sympathetic nerve activity to estimate stellate ganglion nerve activity in dogs.
        Heart Rhythm. 2015; 12: 1324-1332
        • Doytchinova A.
        • Hassel J.L.
        • Yuan Y.
        • Lin H.
        • Yin D.
        • Adams D.
        • et al.
        Simultaneous noninvasive recording of skin sympathetic nerve activity and electrocardiogram.
        Heart Rhythm. 2017; 14: 25-33
        • Sakurai K.
        • Nishi A.
        • Kondo K.
        • Yanagida K.
        • Kawakami N.
        Screening performance of K6/K10 and other screening instruments for mood and anxiety disorders in Japan.
        Psychiatry Clin Neurosci. 2011; 65: 434-441
        • Dietch J.R.
        • Taylor D.J.
        • Sethi K.
        • Kelly K.
        • Bramoweth A.D.
        • Roane BM.
        Psychometric evaluation of the PSQI in U.S. college students.
        J Clin Sleep Med. 2016; 12: 1121-1129
        • Petrakova L.
        • Doering B.K.
        • Vits S.
        • Engler H.
        • Rief W.
        • Schedlowski M.
        • et al.
        Psychosocial stress increases salivary alpha-amylase activity independently from plasma noradrenaline levels.
        PloS ONE. 2015; 10e0134561
        • Tsioufis C.
        • Andrikou I.
        • Thomopoulos C.
        • Syrseloudis D.
        • Stergiou G.
        • Stefanadis C.
        Increased nighttime blood pressure or nondipping profile for prediction of cardiovascular outcomes.
        J Hum Hypertens. 2011; 25: 281-293
        • Sequeira V.C.C.
        • Bandeira P.M.
        • Azevedo JCM.
        Heart rate variability in adults with obstructive sleep apnea: a systematic review.
        Sleep Sci. 2019; 12: 214-221
        • Treptow E.
        • Pepin J.L.
        • Bailly S.
        • Levy P.
        • Bosc C.
        • Destors M.
        • et al.
        Reduction in sympathetic tone in patients with obstructive sleep apnoea: is fixed CPAP more effective than APAP? A randomised, parallel trial protocol.
        BMJ Open. 2019; 9e024253
        • Mongkhonsiri P.
        • Tong-Un T.
        • Wyss J.M.
        • Roysommuti S.
        Blunted nighttime sympathetic nervous system response to stress among Thai men with positive family history of sudden unexplained nocturnal death syndrome.
        Int Heart J. 2019; 60: 55-62
        • Dunn L.K.
        • Kleiman A.M.
        • Forkin K.T.
        • Bechtel A.J.
        • Collins S.R.
        • Potter J.F.
        • et al.
        Anesthesiology resident night float duty alters sleep patterns: an observational study.
        Anesthesiology. 2019; 131: 401-409
        • Tobaldini E.
        • Fiorelli E.M.
        • Solbiati M.
        • Costantino G.
        • Nobili L.
        • Montano N.
        Short sleep duration and cardiometabolic risk: from pathophysiology to clinical evidence.
        Nat Rev Cardiol. 2019; 16: 213-224
        • Fang J.
        • Wheaton A.G.
        • Keenan N.L.
        • Greenlund K.J.
        • Perry G.S.
        • Croft JB.
        Association of sleep duration and hypertension among US adults varies by age and sex.
        Am J Hypertens. 2012; 25: 335-341
        • Ryu J.
        • Jung-Choi K.
        • Choi K.H.
        • Kwon H.J.
        • Kang C.
        • Kim H.
        Associations of shift work and its duration with work-related injury among electronics factory workers in South Korea.
        Int J Environ Res Public Health. 2017; 14: 1429
        • Qian J.
        • Morris C.J.
        • Caputo R.
        • Wang W.
        • Garaulet M.
        • Scheer F.
        Sex differences in the circadian misalignment effects on energy regulation.
        Proc Natl Acad Sci USA. 2019; 116: 23806-23812
        • Valladares E.M.
        • Eljammal S.M.
        • Motivala S.
        • Ehlers C.L.
        • Irwin MR.
        Sex differences in cardiac sympathovagal balance and vagal tone during nocturnal sleep.
        Sleep Med. 2008; 9: 310-316
        • Carter J.R.
        • Ray CA.
        Sympathetic neural adaptations to exercise training in humans.
        Auton Neurosci. 2015; 188: 36-43
        • Zhang P.
        • Liang J.J.
        • Cai C.
        • Tian Y.
        • Dai M.Y.
        • Wong J.
        • et al.
        Characterization of skin sympathetic nerve activity in patients with cardiomyopathy and ventricular arrhythmia.
        Heart Rhythm. 2019; 16: 1669-1675
        • Kusayama T.
        • Wan J.
        • Doytchinova A.
        • Wong J.
        • Kabir R.A.
        • Mitscher G.
        • et al.
        Skin sympathetic nerve activity and the temporal clustering of cardiac arrhythmias.
        JCI Insight. 2019; 4e125853
        • Liu X.
        • Rabin P.L.
        • Yuan Y.
        • Kumar A.
        • Vasallo P.
        • Wong J.
        • et al.
        Effects of anesthetic and sedative agents on sympathetic nerve activity.
        Heart Rhythm. 2019; 16: 1875-1882
        • Kumar A.
        • Wright K.
        • Uceda D.E.
        • Vasallo P.A.
        • Rabin P.L.
        • Adams D.
        • et al.
        Skin sympathetic nerve activity as a biomarker for syncopal episodes during a tilt table test.
        Heart Rhythm. 2019; 17: 804-812
        • Xiao P.L.
        • Cai C.
        • Zhang P.
        • DeSimone C.V.
        • Ernst D.K.
        • Yin Y.H.
        • et al.
        Cardiac resynchronization therapy modulates peripheral sympathetic activity.
        Heart Rhythm. 2020; 17: 1139-1146