The Influence of Exercise and Physical Activity on Autonomic Nervous System Function Measured by Heart Rate Variability in Individuals with Type 1 Diabetes Mellitus—A Systematic Review
Abstract
1. Introduction
2. Materials and Methods
2.1. Search Strategy and Selection of Studies
2.2. Assessment of Methodological Quality and Synthesis
3. Results
3.1. Study Selection
3.2. Study Characteristics
3.3. Methodological Quality
3.4. Results of Individual Studies
3.5. Synthesis of Evidence
4. Discussion
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
HRV | Heart rate variability |
NN | Normal-to-normal intervals |
SDNN | Standard deviation of normal-to-normal intervals |
RMSSD | Sum of squares of differences between adjacent normal-to-normal intervals |
LF | Low frequency |
HF | High frequency |
PRISMA | Preferred Reporting Items for Systematic Reviews and Meta-Analyses |
EPHPP | Effective public health practice project |
ECG | Electrocardiogram |
T1DM | Type 1 diabetes mellitus |
HIIT | High-intensity interval training |
PPO | Peak power output |
PAQ | Physical activity questionnaire |
PA | Physical activity |
METS | Metabolic equivalents |
SED | Sedentary |
LPA | Light physical activity |
MVPA | Moderate-to-vigorous physical activity |
VO2max | Maximum oxygen consumption |
Appendix A. Search String
Database | Search String | Results |
---|---|---|
Pubmed | ((((((((((((((((((((((((((Ketosis-Prone Diabetes Mellitus [Title/Abstract]) OR (Diabetes Mellitus, Ketosis Prone [Title/Abstract])) OR (Diabetes Mellitus, Ketosis-Prone [Title/Abstract])) OR (Brittle Diabetes Mellitus [Title/Abstract])) OR (Diabetes Mellitus, Brittle [Title/Abstract])) OR (Autoimmune Diabetes [Title/Abstract])) OR (Diabetes, Autoimmune [Title/Abstract])) OR (Diabetes Mellitus, Type I [Title/Abstract])) OR (Diabetes, Type 1 [Title/Abstract])) OR (Type 1 Diabetes [Title/Abstract])) OR (Insulin Dependent Diabetes Mellitus 1 [Title/Abstract])) OR (Insulin-Dependent Diabetes Mellitus 1 [Title/Abstract])) OR (Diabetes Mellitus, Insulin-Dependent, 1 [Title/Abstract])) OR (Type 1 Diabetes Mellitus [Title/Abstract])) OR (Sudden-Onset Diabetes Mellitus [Title/Abstract])) OR (Diabetes Mellitus, Sudden Onset [Title/Abstract])) OR (Diabetes Mellitus, Sudden-Onset [Title/Abstract])) OR (Juvenile Onset Diabetes [Title/Abstract])) OR (Diabetes, Juvenile-Onset [Title/Abstract])) OR (Juvenile-Onset Diabetes [Title/Abstract])) OR (IDDM [Title/Abstract])) OR (Juvenile-Onset Diabetes Mellitus [Title/Abstract])) OR (Diabetes Mellitus, Juvenile Onset [Title/Abstract])) OR (Diabetes Mellitus, Juvenile-Onset [Title/Abstract])) OR (Insulin-Dependent Diabetes Mellitus [Title/Abstract])) OR (Diabetes Mellitus, Insulin Dependent [Title/Abstract])) OR (Diabetes Mellitus, Insulin-Dependent [Title/Abstract]) OR “Diabetes Mellitus, Type 1” [Mesh] AND (((((((((((((Autonom* Modu*, Cardia* [Title/Abstract]) OR (Cardia* Autonom* Modu* [Title/Abstract])) OR (Interval*, Inter Beat [Title/Abstract])) OR (Interval*, Inter-Beat [Title/Abstract])) OR (Inter Beat Interval* [Title/Abstract])) OR (Inter-Beat Interval* [Title/Abstract])) OR (Heart-Period Variabilit* [Title/Abstract])) OR (Heart Period Variabilit* [Title/Abstract])) OR (Cycle-Length Variabilit* [Title/Abstract])) OR (Cycle Length Variabilit* [Title/Abstract])) OR (Interval, R-R [Title/Abstract])) OR (R-R Interval [Title/Abstract])) OR (Variabilit*, Heart Rate [Title/Abstract])) OR (Heart Rate Variabilit* [Title/Abstract]) AND”Exercise” [Mesh] OR (((((((((((((((((((((((((((((Exercise*, Endurance [Title/Abstract]) OR (Endurance Exercise* [Title/Abstract])) OR (Training*, Endurance [Title/Abstract])) OR (Endurance Training* [Title/Abstract])) OR (Training*, Strength [Title/Abstract])) OR (Strength Training* [Title/Abstract])) OR (Exercise*, Strength [Title/Abstract])) OR (Strength Exercise* [Title/Abstract])) OR (Workout [Title/Abstract])) OR (Interval Exercise* [Title/Abstract])) OR (Training, Interval* [Title/Abstract])) OR (Interval Training* [Title/Abstract])) OR (High Intensit* Interval* Training* [Title/Abstract])) OR (HIIT [Title/Abstract])) OR (High-Intensity-Interval-Training* [Title/Abstract])) OR (Training*, Resistance [Title/Abstract])) OR (Resistance Training* [Title/Abstract])) OR (Training*, Exercise* [Title/Abstract])) OR (Exercise* Training* [Title/Abstract])) OR (Aerobic Exercise* [Title/Abstract])) OR (Exercise*, Aerobic [Title/Abstract])) OR (Isometric Exercise* [Title/Abstract])) OR (Exercise*, Isometric [Title/Abstract])) OR (Exercise*, Acute [Title/Abstract])) OR (Acute Exercise* [Title/Abstract])) OR (Physical Exercise* [Title/Abstract])) OR (Exercise*, Physical [Title/Abstract])) OR (Activit*, Physical [Title/Abstract])) OR (Physical Activit* [Title/Abstract])) OR (Exercise* [Title/Abstract]) | 55 |
Embase | ‘cycle length variabilit*’:ab,ti OR ‘heart period variabilit*’:ab,ti OR ‘r r interval’:ab,ti OR ‘autonom* modu*, cardia*’:ab,ti OR ‘cardia* autonom* modu*’:ab,ti OR ‘interval*, inter beat’:ab,ti OR ‘inter beat interval*’:ab,ti OR ‘variabilit*, heart rate*’:ab,ti OR ‘heart rate variabilit*’:ab,ti AND ‘exercise*’:ab,ti OR ‘physical activit*’:ab,ti OR ‘endurance training*’:ab,ti OR ‘resistance training*’:ab,ti OR ‘acute exercise*’:ab,ti OR ‘aerobic exercise*’:ab,ti OR ‘isometric exercise*’:ab,ti OR ‘interval training*’:ab,ti OR ‘high intensity* interval training*’ab,ti OR ‘high intensity training*’: ab,ti OR ‘high intensity exercise*’:ab,ti OR ‘interval exercise*’: ab,ti OR ‘HIIT’:ab,ti AND ‘ketosis prone diabetes’:ab,ti OR ‘diabetes mellitus, ketosis prone’:ab,ti OR ‘brittle diabetes mellitus’:ab,ti OR ‘diabetes mellitus, brittle’:ab,ti OR ‘autoimmune diabetes mellitus’:ab,ti OR ‘diabetes, autoimmune’:ab,ti OR ‘Type 1 Diabetes Mellitus’:ab,ti OR ‘Type 1 diabetes’:ab,ti OR ‘Diabetes Type 1’:ab,ti OR ‘Diabetes Mellitus, type 1’:ab,ti OR ‘insuline dependent diabetes mellitus’:ab,ti OR ‘diabetes mellitus, insuline dependent’:ab,ti OR ‘sudden onset diabetes mellitus’:ab,ti OR ‘diabetes mellitus, sudden onset’:ab,ti OR ‘juvenile onset diabetes mellitus’:ab,ti OR ‘juvenile diabetes mellitus’:ab,ti OR ‘IDDM’:ab,ti OR ‘DM1’:ab,ti OR ‘T1DM’:ab,ti OR ‘DMT1’:ab,ti | 49 |
Cochrane |
| |
CINAHL | (MH “Diabetes Mellitus, Type 1”) OR diabetes mellitus type 1 OR insulin dependent diabetes mellitus OR sudden onset diabetes mellitus OR autoimmune diabetes mellitus OR ketosis prone diabetes OR dm1 OR juvenile onset diabetes mellitus OR IDDM OR Type 1 Diabetes Mellitus OR Brittle Diabetes Mellitus AND (MH “Exercise”) OR (MH “Physical Activity”) OR (MH “Physical Fitness”) OR (MH “Leisure Activities”) OR (MH “Physical Performance”) OR (MH “Sports”) OR exercise* OR physical activit* OR endurance training* OR resistance training* OR acute exercise* OR aerobic exercise* OR isometric exercise* OR interval training* OR high intensit* interval training* OR interval exercise* OR high intensity training* OR HIIT AND(MH “Heart Rate Variability”) OR cycle length variabilit* OR heart period variabilit* OR cardia* autonom* modulation OR inter-beat interval OR inter beat interval | 7 |
Appendix B. Heart Rate Variability Parameters
Variables | Units | Description | Interpretation |
---|---|---|---|
Time-domain analysis | |||
Entry 2 | data | Data | |
RR | ms | RR intervals | Basis for analysis |
SDNN | ms | Standard deviation of all NN intervals | Reflect overall variability |
RMSSD | ms | Square root of the mean of the sum of squares of differences between adjacent NN intervals | Reflecting parasympathetic modulation |
MSSD | ms | Mean squared successive differences | |
pNN50 | % | Percentage difference between adjacent NN intervals that are greater than 50 ms | Reflecting parasympathetic modulation |
Frequency-domain analysis | |||
Total Power | ms2 | Variance of all NN intervals < 0.4 Hz | Reflects overall ANS function |
VLF | ms2 | Very low frequency < 0.003–0.04 Hz | Measure of sympathetic activity |
LF | ms2 | Low-frequency power 0.04–0.15 Hz | Sympathetic and parasympathetic activity |
HF | ms2 | High-frequency power 0.15–0.4 Hz | |
LF/HF | |||
Additional | |||
PSD | Power spectral density | ||
CCV | Coefficients of component variance | Power ½ × 100/RR interval mean | |
SNS Index | Sympathetic Nervous System Index | Global Sympathetic Nervous Activity |
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Study Characteristics | Sample | HRV Parameters | Intervention § | Relevant Results | ||||
---|---|---|---|---|---|---|---|---|
Reference | Design † | N total (m/f) | Type | Age ± SD | Method | Variables | ||
Alarcón-Gomez et al. 2021 [49] | Randomized experimental, parallel, open-label trial | 19 (10/9) | I: T1DM C: T1DM | I:38 ± 5.5 C:35 ± 8.2 | Heart Rate Sensor (Polar H10 with Polar Pro strap) | RMSSD LF/HF | Exercise intervention: HIIT training 30 s peak at 85% of PPO 1 min recovery at 40% PPO Duration: 3× per week for 6 weeks C: No exercise | I: RMSSD pre/post conditions 37.8 ± 27.9 vs. 44.3 ± 27.7 (p < 0.05, ES: 0.22) LF/HF pre/post conditions 2.6 ± 1.6 vs. 1.5 ± 0.9 (p < 0.05, ES: 0.23) Significant interaction condition × time in LF/HF (p < 0.05) C: No significant changes in control group RMSSD pre/post conditions 40.0 ± 15.9 vs. 39.3 ± 16.6 LF/HF ratio pre/post conditions 2.1 ± 2.0 vs. 1.9 ± 2.2 |
Saki et al. 2023 [48] | N/R Clinical controlled trial | 36 (36/0) | I: T1DM C1: T1DM C2: Healthy | I: 15.6 ± 1.80 C1: 15.25 ± 1.76 C2: 15.08 ± 1.67 | ECG Holter monitor | SDNN RMSSD HF LF LF/HF | Exercise intervention: HIIT running and swimming 10–15 min w/u, stretching, training and 10 min c/u Running: 30–55 min with 3–6 periods of 5 min at 50–75% HRR and 4 min recovery at 10–20% HRR. Swimming: 10–15 mini front crawl leg, 30–55 min with 3–6 periods of 5 min full front crawl at 50–75% and 4 min recovery at 10–20% of HRR. Resistance training Duration: 3× per week for 12 weeks | Pre-test HRV was significantly different in C2 group compared to I and C1 group. Significant ME in the intervention group for SDNN, RMSSD, LF, HF and LF/HF after intervention. Significant between-group differences after intervention (adjusted means ± SE): I vs. C1: SDNN 137.19 ± 3.00 vs. 135.02 ± 2.33 (p < 0.001) RMSSD 41.10 ± 1.68 vs. 40.86 ± 1.38 (p < 0.001) LF 1465.23 ± 40.26 vs. 1544.64 ± 35.14 (p < 0.001), HF 737.71 ± 45.50 vs. 779.56 ± 29.59 (p < 0.001) LF/HF 2.15 ± 0.05 vs. 2.24 ± 0.03 (p < 0.001) I group improved significantly better than C1 group. I vs. C2: SDNN 137.19 ± 3.00 vs. 156.34 ± 2.23 (p < 0.001) RMSSD 41.10 ± 1.68 vs. 48.38 ± 1.22 (p < 0.001) LF 1465.23 ± 40.26 vs. 2042.48 ± 44.26 (p < 0.001) HF 737.71 ± 45.50 vs. 1312.28 ± 29.29 (p < 0.001) LF/HF 2.15 ± 0.05 vs. 1.37 ± 0.04 (p < 0.001) C2 group was significantly better than I group. No significant differences between C1 and C2 after testing |
Chen et al. 2007 [47] | Retrospective pre/post design | 200 (95/105) | I: T1DM C: Healthy | I:10.3 ± 1.6 C:10.4 ± 1.6 | Three-channel ECG | LF HF LF/HF | I: PAQ-C, in which children were divided into Low (<2), Moderate (>2 and <3) or High (>3) activity levels based on the past 7 days. Stair stepper for 10 min C: Same as I | Significant between-group differences: LnHF (4.9 ± 0.9), LnLF (6.0 ± 0.7) and LnTP (6.7 ± 0.4) significantly ↓ in resting state (p < 0.05). No significant differences in LnHF/LF. In active state, no significant differences between T1DM and controls: LnHF (2.2 ± 1.1 vs. 2.3 ± 1.1), LnLF (4.0 ± 0.9 vs. 4.1 ± 0.8), LnHF/LF (1.7 ± 0.5 vs. 1.7 ± 0.7) and LnTP (5.0 ± 0.8 vs. 5.0 ± 0.7) Significantly decreased within-group changes when going from resting to active state in LnHF, LnLF and LnTP. PA predicted 54% of the variance in HRV parameters (r = −0.21, p < 0.05). |
Javorka et al. 2001 [45] | N/R Prospective cohort study | 20 (N/R) | I: Trained T1DM C: Non-trained T1DM | 15.5 ± 1.2 | ECG signal through chest belt (Varia Pulse TF3 System) | RR MSSD HF LF VLF TP LF/HF VLF/LF LF/HF | Reconditioning summer camp for 8 days including non-mandatory activities: table tennis, badminton, 3–5 km distance walking, hiking, swimming 2× per day. Self-reported weekly physical activity levels for the last 6 months. C: Same as I | Trained subgroup compared to non-trained group had significantly longer RR intervals, ↑MSSD, VLF, HF and LF↑ (p < 0.05). Abnormal HRV parameters in 14.6 ± 6% of trained individuals vs. 54 ± 9% in untrained. Significant changes before and after with n total. No relevant differences between trained and untrained group (p < 0.05): RR↑ (715 ± 23 vs. 786 ± 22) MSDD↑ (2103 ± 714 vs. 6072 ± 1603) HF↑ (1024 ± 411 vs. 2195 ± 547) Rel.P.VLF↓ (47.6 ± 3.6 vs. 33.5 ± 4.1) Rel.P.HF↑ (30.4 ± 4.1 vs. 47.9 ± 5.1) VLF/HF↓ (2.8 ± 0.6 vs. 1.1 ± 0.3) |
Lucini et al. 2012 [44] | N/R Prospective cohort study | 77 (50/27) | T1DM | 15.0 ± 0.6 | Two-way radio telemetry system (Finapres) | RR VARRR LFRR HFRR LF/HFRR Units used: ms and nu | METS calculation through assessment of time spent walking (>10 min) and/or exercise (structured or leisure time). At T1, subgroups were designated according to increased (Group 1), unchanged (Group 2) or diminished (Group 3) total weekly METS. | Significant interaction of between-group results in RR (p = 0.04), LFRR [nu] (p = 0.03) and HFRR [nu] (p = 0.01). Group 1: RR↑ (835. 1 ± 24.7 vs. 885.6 ± 23.2), VAR↑ (4443 ± 703 vs. 5042 ± 755), LF(ms)↓ (1176 ± 220 vs. 1152 ± 170), LF(nu)↓ (44.2 ± 3.2 vs. 41.1 ± 3.2) HF(ms)↑ (1918 ± 436 vs. 2425 ± 533), HF(nu)↑ (47.8 ± 2.9 vs. 52.6 ± 3.0) LF/HF↓(1.5 ± 0.3 vs. 1.1 ± 0.2) Exercise amount ↑ (METS/p.m/p.w.) is associated with a small reduction in LFRR and increase in HFRR. |
Marshall et al. 2021 [46] | N/R Prospective cohort study | 37 (21/16) | I: T1DM C: Non-diabetic subjects | I: 11.9 ± 1.5 C:11.6 ± 2.2 | ECG | RMSSD LF HF | Triaxial accelerometer measurement for 28 days, 24 h p.d. SED, LPA, MVPA and sleep time were determined. C: Same as I | RMSSD is significantly negatively associated with SED (γ = −28.94, p < 005) and non-significantly negatively associated with MVPA (γ = −3.06, p > 0.05). Positive association with LPA (γ = 18.13) and sleep (γ = 13.87), both non-significant (p > 0.05). LF was negatively associated with SED (γ = −2.25), MVPA (γ = −1.76) and LPA (γ = −8.09) (non-significant). Positive association with sleep (γ = 12.10) HF was only negatively associated with sleep (γ = −12.04) but positively associated with SED (γ = 2.24), LPA (γ = 8.05) and MVPA (γ = 1.75) (non-significant). |
Shin et al. 2014 [50] | N/R Prospective cohort study | 15 (15/0) | T1DM | 13.0 ± 1.0 | ECG monitor | TP VLF LF HF SNS index | Walking exercise program 3× p.w. for 12 weeks. Exercise intensity was set at 60% of VO2max. Duration requirement was at least 250 kcal per exercise session. | Pre/post HRV power analysis parameters all increased significantly (p < 0.05): TP (998.46 ± 232.2 vs. 1587.47 ± 449.25) LF (541.26 ± 187.59 vs. 942.22 ± 397.84) VLF (128.11 ± 58.66 vs. 389.44 ± 198.55) SNS index and HF power were not significantly different before and after testing. |
Study | 1 | 2 | 3 | 4 | 5 | 6 | Global Rating |
---|---|---|---|---|---|---|---|
Alarcón-Gómez et al. [49] | ~ | − | + | − | + | ~ | Weak |
Chen et al. [47] | ~ | − | + | − | + | − | Weak |
Javorka et al. [45] | − | − | + | − | − | − | Weak |
Lucini et al. [44] | ~ | − | − | − | + | − | Weak |
Marshall et al. [46] | ~ | − | + | − | + | ~ | Weak |
Saki et al. [48] | − | − | + | ~ | + | − | Weak |
Shin et al. [50] | − | − | + | − | + | − | Weak |
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Bekker, I.; Kooistra, A.; van Dijk, P.R.; Lefrandt, J.D.; Veeger, N.J.G.M.; van Beek, A.P. The Influence of Exercise and Physical Activity on Autonomic Nervous System Function Measured by Heart Rate Variability in Individuals with Type 1 Diabetes Mellitus—A Systematic Review. Int. J. Mol. Sci. 2025, 26, 7096. https://doi.org/10.3390/ijms26157096
Bekker I, Kooistra A, van Dijk PR, Lefrandt JD, Veeger NJGM, van Beek AP. The Influence of Exercise and Physical Activity on Autonomic Nervous System Function Measured by Heart Rate Variability in Individuals with Type 1 Diabetes Mellitus—A Systematic Review. International Journal of Molecular Sciences. 2025; 26(15):7096. https://doi.org/10.3390/ijms26157096
Chicago/Turabian StyleBekker, Isabel, Arne Kooistra, Peter R. van Dijk, Joop D. Lefrandt, Nic J. G. M. Veeger, and André P. van Beek. 2025. "The Influence of Exercise and Physical Activity on Autonomic Nervous System Function Measured by Heart Rate Variability in Individuals with Type 1 Diabetes Mellitus—A Systematic Review" International Journal of Molecular Sciences 26, no. 15: 7096. https://doi.org/10.3390/ijms26157096
APA StyleBekker, I., Kooistra, A., van Dijk, P. R., Lefrandt, J. D., Veeger, N. J. G. M., & van Beek, A. P. (2025). The Influence of Exercise and Physical Activity on Autonomic Nervous System Function Measured by Heart Rate Variability in Individuals with Type 1 Diabetes Mellitus—A Systematic Review. International Journal of Molecular Sciences, 26(15), 7096. https://doi.org/10.3390/ijms26157096