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Association of Self-reported Walking Pace With Type 2 Diabetes Incidence in the UK Biobank Prospective Cohort Study

      Abstract

      Objective

      To investigate the association between self-reported walking pace and type 2 diabetes (T2D) incidence and whether it differed by physical activity levels and walking time.

      Methods

      There were 162,155 participants (mean age, 57.1 years; 54.9% women) from the UK Biobank prospective study, recruited between 2006 and 2010, included in the study. Walking pace was self-reported and classified as brisk, average, or slow. Total physical activity and walking time were self-reported using the International Physical Activity Questionnaire. Association between walking pace and T2D incidence and the potential moderating role of physical activity and walking time were investigated using Cox proportional hazards models.

      Results

      The median follow-up was 7.4 (interquartile range, 6.7 to 8.2) years. There were 4442 participants in whom T2D developed during the follow-up period. In the fully adjusted model (sociodemographic factors, diet, body mass index, and physical activity), average walking pace (hazard ratio [HR], 1.28; 95% CI, 1.14 to 1.44) and slow walking pace (HR, 1.91; 95% CI, 1.62 to 2.24) were associated with a higher T2D risk compared with brisk walking among women. Among men, average walking pace (HR, 1.28; 95% CI, 1.17 to 1.40) and slow walking pace (HR, 1.73; 95% CI, 1.50 to 1.99) were also associated with higher T2D risk. Compared with slow walkers, brisk walkers have the same diabetes incidence rate 18.6 and 16.0 years later, for women and men, respectively.

      Conclusion

      Average and slow walking pace was associated with a higher risk of incident T2D in both men and women, independent of major confounding factors. The associations were consistent across different physical activity levels and walking time.

      Abbreviations and Acronyms:

      BMI (body mass index), CVD (cardiovascular disease), HR (hazard ratio), T2D (type 2 diabetes)
      Type 2 diabetes (T2D) is a current major public health challenge linked to a higher risk of noncommunicable diseases, such as cardiovascular disease (CVD), chronic kidney disease, and premature death. In 2017, people affected by T2D accounted for 6.2% of the worldwide population.
      • Khan M.A.
      • Hashim M.J.
      • King J.K.
      • Govender R.D.
      • Mustafa H.
      • Al Kaabi J.
      Epidemiology of type 2 diabetes—global burden of disease and forecasted trends.
      Moreover, people with T2D live, on average, 4 to 10 years less than those without.
      • Chan J.C.
      • Lim L.L.
      • Wareham N.J.
      • et al.
      The Lancet Commission on diabetes: using data to transform diabetes care and patient lives.
      There is emerging evidence on the role of lifestyle in preventing T2D as well as in preventing the complications and comorbidities associated with T2D.
      • Chan J.C.
      • Lim L.L.
      • Wareham N.J.
      • et al.
      The Lancet Commission on diabetes: using data to transform diabetes care and patient lives.
      Physical activity is a key lifestyle factor for the prevention and treatment of T2D.
      • Chan J.C.
      • Lim L.L.
      • Wareham N.J.
      • et al.
      The Lancet Commission on diabetes: using data to transform diabetes care and patient lives.
      Existing evidence from randomized controlled trials and prospective cohort studies highlights the beneficial effect of physical activity on T2D. However, most of this evidence is based on total physical activity or leisure-time physical activity,
      • Smith A.D.
      • Crippa A.
      • Woodcock J.
      • Brage S.
      Physical activity and incident type 2 diabetes mellitus: a systematic review and dose-response meta-analysis of prospective cohort studies.
      ,
      Physical Activity Guidelines Advisory Committee
      2018 Physical Activity Guidelines Advisory Committee Scientific Report.
      with less evidence available for specific forms of physical activity, such as walking, and the importance of people’s habitual walking pace.
      • Hamasaki H.
      Daily physical activity and type 2 diabetes: a review.
      • Hall K.S.
      • Hyde E.T.
      • Bassett D.R.
      • et al.
      Systematic review of the prospective association of daily step counts with risk of mortality, cardiovascular disease, and dysglycemia.
      • Iwasaki M.
      • Kudo A.
      • Asahi K.
      • et al.
      Fast walking is a preventive factor against new-onset diabetes mellitus in a large cohort from a Japanese general population.
      Studies have suggested that a slow walking pace is a strong predictor of poorer health outcomes, including CVD, respiratory diseases, cancer, and all-cause mortality.
      • Celis-Morales C.A.
      • Gray S.
      • Petermann F.
      • et al.
      Walking pace is associated with lower risk of all-cause and cause-specific mortality.
      ,
      • Welsh C.E.
      • Celis-Morales C.A.
      • Ho F.K.
      • et al.
      Grip strength and walking pace and cardiovascular disease risk prediction in 406,834 UK Biobank participants.
      Despite this, most of the evidence on walking pace and T2D risk comes from cross-sectional studies,
      • Cigarroa I.
      • Espinoza-Sanhueza M.
      • Lasserre Laso N.
      • et al.
      Association between walking pace and diabetes: findings from the Chilean National Health Survey 2016-2017.
      with the few existing prospective studies having a relatively small sample size. Many did not address whether the associations were independent of total physical activity.
      • Hall K.S.
      • Hyde E.T.
      • Bassett D.R.
      • et al.
      Systematic review of the prospective association of daily step counts with risk of mortality, cardiovascular disease, and dysglycemia.
      ,
      • Iwasaki M.
      • Kudo A.
      • Asahi K.
      • et al.
      Fast walking is a preventive factor against new-onset diabetes mellitus in a large cohort from a Japanese general population.
      ,
      • Hu F.B.
      • Sigal R.J.
      • Rich-Edwards J.W.
      • et al.
      Walking compared with vigorous physical activity and risk of type 2 diabetes in women a prospective study.
      • Hu F.B.
      • Leitzmann M.F.
      • Stampfer M.J.
      • Colditz G.A.
      • Willett W.C.
      • Rimm E.B.
      Physical activity and television watching in relation to risk for type 2 diabetes mellitus in men.
      • Krishnan S.
      • Rosenberg L.
      • Palmer J.R.
      Physical activity and television watching in relation to risk of type 2 diabetes: the Black Women's Health Study.
      • Caspersen C.J.
      • Fulton J.E.
      Epidemiology of walking and type 2 diabetes.
      It is therefore unclear whether any association between walking pace and T2D is consistent among people with different physical activity levels and walking times.
      • Smith A.D.
      • Crippa A.
      • Woodcock J.
      • Brage S.
      Physical activity and incident type 2 diabetes mellitus: a systematic review and dose-response meta-analysis of prospective cohort studies.
      ,
      • Kelly P.
      • Kahlmeier S.
      • Götschi T.
      • et al.
      Systematic review and meta-analysis of reduction in all-cause mortality from walking and cycling and shape of dose response relationship.
      Such information will be useful to optimize walking-based interventions for T2D and to identify people who are at higher T2D risk. Therefore, to address these gaps in the literature, the aim of this study was to investigate the association between self-reported walking pace and risk of T2D and whether this association differs by total physical activity and walking time in the UK Biobank, a large prospective cohort study.

      Methods

      Study Cohort

      The UK Biobank recruited more than 502,000 participants between 2006 and 2010 (5.5% response rate; men and women were aged 37 to 73 years) from the general population (Supplemental Figure 1).
      • Collins R.
      What makes UK Biobank special?.
      Participants attended 1 of 22 assessment centers across England, Wales, and Scotland.
      • Sudlow C.
      • Gallacher J.
      • Allen N.
      • et al.
      UK Biobank: an open access resource for identifying the causes of a wide range of complex diseases of middle and old age.
      At the assessment centers, they completed an electronically signed consent and detailed information about their sociodemographic characteristics and lifestyles with physical measurements.
      • Sudlow C.
      • Gallacher J.
      • Allen N.
      • et al.
      UK Biobank: an open access resource for identifying the causes of a wide range of complex diseases of middle and old age.
      Analyses for this study were conducted in participants of the UK Biobank cohort who had available records for T2D incidence from primary care records, the exposure of interest (self-reported walking pace), and all covariates. Participants with prevalent type 1 diabetes, T2D, or undiagnosed diabetes (hemoglobin A1c level ≥48 mmol/mol) at the baseline assessment were excluded from the study.

      Ethical Approval

      The UK Biobank study was approved by the North West Multi-Centre Research Ethics Committee (Ref 11/NW/0382 on June 17, 2011), and all participants provided written informed consent to participate in the UK Biobank study. The study protocol is available online (http://www.ukbiobank.ac.uk/).

      Outcome

      Incident T2D was derived from linkage to primary care data in the UK Biobank. Records were extracted for 45% of the UK Biobank cohort (228,495 participants). The end of coverage (extract date) was May 2017 for Scotland, September 2017 for Wales, and August 2017 for England. Detailed linkage procedures are described elsewhere.
      UK Biobank
      Category 3000. Primary care—health-related outcomes.
      We defined incident T2D as primary care diagnosed with International Classification of Diseases, Tenth Revision (ICD-10) code E11. Read codes used in the primary care data were converted into ICD-10 codes using UK Biobank's look-up table.

      Exposure

      Participants self-reported their usual walking pace on a touch-screen questionnaire at the baseline assessment visit. The question asked was, How would you describe your usual walking pace? Participants could select 1 of the 3 following options: brisk (>4 miles/hour), average (3-4 miles/hour), or slow (<3 miles/hour) walking pace, as described elsewhere.
      • Celis-Morales C.A.
      • Gray S.
      • Petermann F.
      • et al.
      Walking pace is associated with lower risk of all-cause and cause-specific mortality.
      ,
      • Welsh C.E.
      • Celis-Morales C.A.
      • Ho F.K.
      • et al.
      Grip strength and walking pace and cardiovascular disease risk prediction in 406,834 UK Biobank participants.
      Walking pace in this study was categorized into brisk, average, and slow pace.

      Covariates

      Sex and education were self-reported at baseline; age was calculated from dates of birth and baseline assessment; ethnicity was self-reported at baseline and was categorized as White, South Asian, mixed, Black, and Chinese. Deprivation index, an area-based measure of socioeconomic status, was derived from the postal code of residence using the Townsend deprivation score.
      • Townsend N.P.
      • Phillimore P.
      • Beattie A.
      Health and Deprivation: Inequality and the North.
      Anthropometric measurements were obtained by trained personnel following standard operating procedures and using calibrated equipment.
      UK Biobank
      UK Biobank: Protocol for a large-scale prospective epidemiological resource.
      Body mass index (BMI) was calculated from body weight (in kilograms) divided by square of height (in meters) based on World Health Organization criteria.
      Smoking status was categorized into never, former, and current. Fruit and vegetable intake, red meat intake, and processed meat intake were recorded by using a touch-screen questionnaire asking the reported frequency of consumption at baseline. Alcohol intake was self-reported and categorized into daily/almost daily, 3 or 4 times a week, once or twice a week, 1 to 3 times a month, special occasions only, and never. Sedentary behavior was self-reported, derived from combined TV viewing, leisure PC screen time, and driving time in hours per day.
      • Celis-Morales C.A.
      • Lyall D.M.
      • Steell L.
      • et al.
      Associations of discretionary screen time with mortality, cardiovascular disease and cancer are attenuated by strength, fitness and physical activity: findings from the UK Biobank study.
      Sleep duration was self-reported and categorized as short sleep, normal sleep, and long sleep. Prevalent diseases that were medically diagnosed were self-reported at baseline.
      Physical activity and walking time were estimated based on the International Physical Activity Questionnaire short form,
      • Celis-Morales C.A.
      • Lyall D.M.
      • Steell L.
      • et al.
      Associations of discretionary screen time with mortality, cardiovascular disease and cancer are attenuated by strength, fitness and physical activity: findings from the UK Biobank study.
      with participants reporting the frequency and duration of walking and moderate and vigorous activity undertaken in a typical week. Total physical activity was computed as the sum of walking and moderate and vigorous activity, measured as metabolic equivalent of task (MET), and people were defined as physically inactive if total physical activity was less than 600 MET-min/wk.
      World Health Organization
      Global Physical Activity Questionnaire (GPAQ) Analysis Guide.
      Additional details about these measurements can be found in the UK Biobank online protocol.
      UK Biobank
      UK Biobank: Protocol for a large-scale prospective epidemiological resource.

      Statistical Analyses

      Descriptive characteristics of the cohort were presented by categories of self-reported walking pace and sex. Continuous variables were presented as mean and standard deviation, whereas categorical variables were presented as the number of observations and their respective percentage.
      Cox proportional hazards models were used to investigate the associations between self-reported walking pace (slow, average, and brisk pace [reference category]) and incident T2D for men and women, separately. The results are reported as hazard ratios (HRs) together with 95% CI. To minimize reverse causation, the analyses were conducted with a 2-year landmark period, excluding events in the first 2 years of the follow-up period, and excluded all participants with prevalent type 1 diabetes, T2D, or undiagnosed T2D (hemoglobin A1c level ≥48 mmol/mol) at the baseline assessment as well as those with missing data on walking pace, physical activity, walking time, and covariates.
      We ran 4 models that included an increasing number of covariates. Model 0 (minimally adjusted) included age, ethnicity, deprivation index, and education. Model 1 (lifestyle model) was adjusted as in model 0 but also included smoking, fruit and vegetable intake, red meat intake, processed meat intake, alcohol intake, total sedentary time, and sleep time. Model 2 (BMI model) was adjusted as in model 1 but also included BMI. Model 3 (fully adjusted) was similar to model 2 but was additionally adjusted for total physical activity. All of the 4 models included walking pace as the exposure variable.
      Interaction analyses were conducted to investigate whether the association between walking pace and risk of subsequent T2D differed by total physical activity level and walking time. An interaction between walking pace category and total physical activity and walking time coded as tertiles were added to the Cox regression analyses, which used brisk walking pace and high physical activity tertile as the reference group (brisk pace/high physical activity). These analyses were adjusted for model 3 but excluded total physical activity as a covariate.
      We calculated rate advancement periods
      • Brenner H.
      • Gefeller O.
      • Greenland S.
      Risk and rate advancement periods as measures of exposure impact on the occurrence of chronic diseases.
      to estimate the number of additional chronologic years that would be required to yield the equivalent risk rate of T2D incidence among individuals who reported a slow walking pace compared with those who reported a brisk walking pace. We divided the coefficient of incidence for those individuals in the slow walking pace category referent to individuals in the brisk walking category by the coefficient for incidence associated with each yearly increase in age, as described elsewhere.
      • Discacciati A.
      • Bellavia A.
      • Orsini N.
      • Greenland S.
      On the interpretation of risk and rate advancement periods.
      We checked the proportional hazard assumption by a test based on Schoenfeld residuals. Statistical analyses were performed using the statistical software Stata 16 (StataCorp LLC). Associations were regarded as significant when P value was less than .05.

      Results

      This study included 162,155 (73,084 men and 89,071 women) participants with complete data for T2D incidence, walking pace, and covariates. The median follow-up period was 7.4 years (interquartile range, 6.7 to 8.2 years). During the follow-up, T2D developed in 4442 participants (2645 men and 1797 women).
      The primary cohort characteristics by walking pace categories are presented in Table 1. In summary, brisk walkers were younger, were more affluent, and had higher education levels than those who reported a slow walking pace. In terms of lifestyle, brisk walkers were leaner, consumed less alcohol and processed meat, ate more fruit and vegetables, spent less time in sedentary behaviors, were more active, and had higher levels of grip strength than slow walkers. A higher proportion of brisk walkers than slow walkers reported being never smokers and had normal sleep hours (7 to 9 h/d). Cohort characteristics by sex are presented in Supplemental Tables 1 and 2 (available online at http://www.mayoclinicproceedings.org).
      Table 1Cohort Characteristics by Self-reported Walking Pace Categories
      CharacteristicsSlow paceAverage paceBrisk pace
      Participants, n816483,18170,810
      Age, years58.8 (7.7)57.1 (8.0)55.3 (8.1)
      Townsend deprivation index, n (%)
       Lower deprivation1839 (22.5)27,976 (33.6)25,868 (36.5)
       Middle deprivation2435 (29.8)28,684 (34.5)24,685 (34.9)
       Higher deprivation3890 (47.7)26,521 (31.9)20,257 (28.6)
      Ethnicity, n (%)
       White7474 (91.6)79,551 (95.6)68,972 (97.4)
       Mixed186 (2.3)938 (1.1)688 (1.0)
       South Asian338 (4.1)1582 (1.9)595 (0.8)
       Black127 (1.6)867 (1.0)456 (0.6)
       Chinese39 (0.5)243 (0.3)99 (0.1)
      Education, n (%)
       College or university degree2182 (39.8)29,539 (44.0)32,411 (51.5)
       A levels/AS levels or equivalent721 (13.2)8725 (13.0)8737 (13.9)
       O levels/GCSEs or equivalent1579 (28.8)18,371 (27.3)14,474 (23.0)
       SEs or equivalent/NVQ or HND or HNC1000 (18.2)10,576 (15.7)7296 (11.6)
      Smoking status, n (%)
       Never3722 (45.6)45,379 (54.6)41,447 (58.5)
       Previous3062 (37.5)29,161 (35.1)23,411 (33.1)
       Current1380 (16.9)8641 (10.4)5952 (8.4)
      Sleep categories, n (%)
       Normal (7-9 h/d)5146 (63.0)62,381 (75.0)54,196 (76.5)
       Short sleep (<7 h/d)2550 (31.2)19,518 (23.5)16,008 (22.6)
       Long sleep (>9 h/d)468 (5.7)1282 (1.5)606 (0.7)
      Diet and lifestyle
       Alcohol intake, n (%)
      Daily or almost daily1308 (16.0)16,493 (19.8)15,935 (22.5)
      3-4 times a week1260 (15.4)19,214 (23.1)19,234 (27.2)
      Once or twice a week1882 (23.1)22,439 (27.0)18,575 (26.2)
      1-3 times a month965 (11.8)9518 (11.4)7357 (10.4)
      Special occasions only1438 (17.6)9365 (11.3)5889 (8.3)
      Never1311 (16.1)6150 (7.4)3819 (5.4)
       Processed meat intake, portion/week, mean (SD)2 (1.1)1.89 (1.1)1.73 (1.1)
       Fruit and vegetable intake, g/d, mean (SD)316.4 (211.4)324.1 (188.6)352.9 (194.6)
       Red meat intake, portion/week, mean (SD)2.2 (1.6)2.2 (1.4)2.0 (1.4)
       Total sedentary time, h/d, mean (SD)5.5 (2.6)5.1 (2.2)4.7 (2.1)
       Total physical activity, MET-h/wk, mean (SD)2007.5 (2436.8)2828.0 (3052.5)3117.1 (3187.1)
       Grip strength, kg, mean (SD)26.3 (11.1)30.4 (10.9)32.2 (10.8)
       Systolic blood pressure, mm Hg, mean (SD)139.7 (18.9)139.1 (18.8)136.2 (18.5)
      Adiposity
       Waist circumference, cm, mean (SD)97.3 (14.3)90.8 (12.7)85.8 (11.8)
       BMI, kg/m2, mean (SD)30.4 (6.1)27.7 (4.5)25.8 (3.7)
       BMI category, n (%)
      Underweight (<18.5 kg/m2)38 (0.5)305 (0.4)504 (0.7)
      Normal (18.5-24.9 kg/m2)1382 (16.9)22,971 (27.6)31,854 (45.0)
      Overweight (25-29.9 kg/m2)2852 (34.9)38,041 (45.7)29,869 (42.2)
      Obese (≥30.0 kg/m2)3892 (47.7)21,864 (26.3)8583 (12.1)
      BMI, body mass index; MET, metabolic equivalent of task.
      Data are presented as mean (SD) for continuous variables and as frequency (%) for categorical variables.
      The association between walking pace and incident T2D is presented in Figure 1. There was a dose-response association between walking pace and T2D risk across all models. For women, using a minimally adjusted model (adjusted for sociodemographic factors), risk of T2D was 2 times (HR, 2.04; 95% CI, 1.82 to 2.29) and 4.8 times (HR, 4.82; 95% CI, 4.13 to 5.61) higher for average and slow women compared with brisk walkers, respectively. For men, T2D risk was 1.7 times (HR, 1.71; 95% CI, 1.56 to 1.87) and 3.1 times (HR, 3.14; 95% CI, 2.74 to 3.60) higher for average and slow walkers compared with brisk walkers. When the analyses were additionally adjusted for lifestyle factors (model 1), the magnitude of the associations was slightly attenuated for both men and women but remained significant (Figure 1). Further adjustment for BMI (model 2) attenuated the magnitude of the associations considerably but remained significant. For women, compared with brisk walkers, average and slow walkers had 29% (HR, 1.29; 95% CI, 1.15 to 1.45) and 94% (HR, 1.94; 95% CI, 1.65 to 2.27) higher risks of T2D, respectively. For men, average and slow walkers had 29% (HR, 1.29; 95% CI, 1.18 to 1.41) and 80% (HR, 1.80; 95% CI, 1.57 to 2.07) higher risk of T2D, respectively. Further adjustment for total physical activity (model 3) did not alter the associations (Figure 1).
      Figure thumbnail gr1
      Figure 1Association between self-reported walking pace and type 2 diabetes incidence in women and men. Data are presented as hazard ratio (HR) and 95% CI by self-reported walking pace categories. Brisk walkers were the reference group (Ref.). Model 0 (minimally adjusted) included age, ethnicity, deprivation index, and education. Model 1 was adjusted as in model 0 but also included smoking, fruit and vegetable intake, red meat intake, processed meat intake, alcohol intake, total sedentary time, and sleep time. Model 2 was adjusted as in model 1 but also included body mass index (BMI). Model 3 (fully adjusted) was similar to model 2 but was additionally adjusted for total physical activity (PA).
      The interactions of walking pace with total physical activity and walking time are shown in Figure 2 and Supplemental Tables 3 and 4 (available online at http://www.mayoclinicproceedings.org). Although no significant interactions were observed for walking pace with either total physical activity or total walking time, T2D risk increased in a dose-response manner among average and slow pace walkers when their physical activity levels decreased. Similar results were observed when walking pace was presented by walking time (Figure 2).
      Figure thumbnail gr2
      Figure 2Association of self-reported walking pace with diabetes risk by total physical activity (PA) and walking time levels in women and men. Data are presented as hazard ratio (HR) and 95% CI. Brisk walkers with high levels of physical activity or walking time were set as the reference group (Ref.). The analyses were adjusted for age, ethnicity, deprivation index, education, smoking, fruit and vegetable intake, red meat intake, processed meat intake, alcohol intake, total sedentary time, sleep time, and body mass index.
      The rate advancement period analysis revealed that slow walkers have higher T2D incidence rates than brisk walkers. For brisk walkers to yield similar incidence rates to those observed for slow walkers, they would be 18.6 and 16.0 years older, for women and men, respectively. Incident rates for average vs slow walkers are presented in Table 2.
      Table 2Advance Rate Period for Incident T2D in Women and Men by Self-reported Walking Pace Category
      RAP for T2D incidence (95% CI)
      Walking pace categoryWomenMen
      Brisk paceReferenceReference
      Average pace7.2 (4.6-8.9)7.2 (5.4-8.6)
      Slow pace18.6 (17.1-19.6)16.0 (14.0-17.4)
      RAP, rate advancement period; T2D, type 2 diabetes.
      Estimate based on hazard ratios shown for model 3 in Figure 1.

      Discussion

      The main finding of this study is that compared with brisk walking, average and slow walking paces were associated with a higher incidence of T2D in both men and women, independent of sociodemographic factors, diet, adiposity, and physical activity level. Among people with average and slow walking paces, high levels of physical activity did not attenuate the excess T2D risk attributable to slow walking pace. We also provide evidence that on average, slow walkers will experience an equivalent T2D incidence rate to that of brisk walkers, but this will occur approximately 18 and 16 years earlier for women and men, respectively. Future studies are needed to verify whether self-reported walking pace could be a useful marker to identify those individuals in whom T2D is more likely to develop, especially if we consider that current evidence suggests that walking pace could improve CVD risk prediction.
      • Welsh C.E.
      • Celis-Morales C.A.
      • Ho F.K.
      • et al.
      Grip strength and walking pace and cardiovascular disease risk prediction in 406,834 UK Biobank participants.
      A few prospective studies that investigated the association of walking pace with incident T2D
      • Iwasaki M.
      • Kudo A.
      • Asahi K.
      • et al.
      Fast walking is a preventive factor against new-onset diabetes mellitus in a large cohort from a Japanese general population.
      ,
      • Hu F.B.
      • Sigal R.J.
      • Rich-Edwards J.W.
      • et al.
      Walking compared with vigorous physical activity and risk of type 2 diabetes in women a prospective study.
      ,
      • Hu F.B.
      • Leitzmann M.F.
      • Stampfer M.J.
      • Colditz G.A.
      • Willett W.C.
      • Rimm E.B.
      Physical activity and television watching in relation to risk for type 2 diabetes mellitus in men.
      were generally consistent with our findings. The Nurses' Health Study investigated the association between walking pace and T2D risk in 70,102 women aged 40 to 60 years who were followed up for 8 years.
      • Hu F.B.
      • Sigal R.J.
      • Rich-Edwards J.W.
      • et al.
      Walking compared with vigorous physical activity and risk of type 2 diabetes in women a prospective study.
      The investigators found that people with normal (or average) and brisk (or very brisk) walking pace were at a lower risk of T2D (relative risk [RR], 0.72 [95% CI, 0.62 to 0.85] and 0.41 [95% CI, 0.33 to 0.52], respectively) compared with those with a slow walking pace.
      • Hu F.B.
      • Sigal R.J.
      • Rich-Edwards J.W.
      • et al.
      Walking compared with vigorous physical activity and risk of type 2 diabetes in women a prospective study.
      However, the authors reported that after adjustment for BMI, although the association between brisk walking pace and T2D risk was attenuated (RR, 0.59; 95% CI, 0.47 to 0.73), the association for average walking pace was no longer present (RR, 0.86; 95% CI, 0.73 to 1.01).
      • Hu F.B.
      • Sigal R.J.
      • Rich-Edwards J.W.
      • et al.
      Walking compared with vigorous physical activity and risk of type 2 diabetes in women a prospective study.
      This disagrees with our findings as the association between average-pace walkers and T2D risk was independent of BMI. Another study conducted in 37,918 men aged 40 to 75 years who were free of diabetes, CVD, and cancer at baseline reported a strong association between walking pace and risk of T2D independent of time spent walking.
      • Hu F.B.
      • Leitzmann M.F.
      • Stampfer M.J.
      • Colditz G.A.
      • Willett W.C.
      • Rimm E.B.
      Physical activity and television watching in relation to risk for type 2 diabetes mellitus in men.
      After adjustment for age, smoking, family history of T2D, alcohol intake, and diet, the risk ratios for normal, brisk, and very brisk pace were 0.68, 0.46, and 0.39, respectively, compared with those who reported an easy or casual pace.
      • Hu F.B.
      • Leitzmann M.F.
      • Stampfer M.J.
      • Colditz G.A.
      • Willett W.C.
      • Rimm E.B.
      Physical activity and television watching in relation to risk for type 2 diabetes mellitus in men.
      Another study conducted in 197,825 nondiabetic Japanese people reported that brisk walking pace was inversely associated with a lower probability of T2D (odds ratio, 0.93; 95% CI, 0.88 to 0.98).
      • Iwasaki M.
      • Kudo A.
      • Asahi K.
      • et al.
      Fast walking is a preventive factor against new-onset diabetes mellitus in a large cohort from a Japanese general population.
      However, when the associations were stratified by sex, age, and BMI, brisk walking was associated with a lower risk of T2D only in participants younger than 65 years, with BMI above 25 kg/m2, and who were men.
      • Iwasaki M.
      • Kudo A.
      • Asahi K.
      • et al.
      Fast walking is a preventive factor against new-onset diabetes mellitus in a large cohort from a Japanese general population.
      Our findings confirmed the inverse association between walking pace and T2D risk, independent of BMI and total physical activity. However, we also provide further evidence that the association between walking pace and T2D risk is also independent of walking time. This has important implications as the detrimental association between slow walking pace and risk of T2D is not attenuated by high levels of physical activity. Previous studies looking at the association of walking pace with other health outcomes, such as CVD, cancer, respiratory diseases, and premature mortality, have also reported that slow walking pace is a strong risk factor independent of other major risk factors, such as poor lifestyle and adiposity.
      • Celis-Morales C.A.
      • Gray S.
      • Petermann F.
      • et al.
      Walking pace is associated with lower risk of all-cause and cause-specific mortality.
      ,
      • Welsh C.E.
      • Celis-Morales C.A.
      • Ho F.K.
      • et al.
      Grip strength and walking pace and cardiovascular disease risk prediction in 406,834 UK Biobank participants.
      ,
      • Ganna A.
      • Ingelsson E.
      5 year mortality predictors in 498 103 UK Biobank participants: a prospective population-based study.
      These studies have also reported that slow walkers are more likely to be pre-frail or frail
      • Petermann-Rocha F.
      • Gray S.R.
      • Pell J.P.
      • Ho F.K.
      • Celis-Morales C.
      The joint association of sarcopenia and frailty with incidence and mortality health outcomes: a prospective study.
      ,
      • Petermann-Rocha F.
      • Pell J.P.
      • Celis-Morales C.
      • Ho F.K.
      Frailty, sarcopenia, cachexia and malnutrition as comorbid conditions and their associations with mortality: a prospective study from UK Biobank. J Public Health (Oxf).
      and to have low cardiorespiratory fitness.
      • Yates T.
      • Zaccardi F.
      • Dhalwani N.N.
      • et al.
      Association of walking pace and handgrip strength with all-cause, cardiovascular, and cancer mortality: a UK Biobank observational study.
      ,
      • Zaccardi F.
      • Davies M.J.
      • Khunti K.
      • Yates T.
      Comparative relevance of physical fitness and adiposity on life expectancy: a UK Biobank observational study.
      However, it is not certain whether walking pace is a causal factor or a marker of risk. Because total physical activity was adjusted in the analysis, the walking pace could be an indicator of overall physical capability/health status. However, it is also possible that higher intensity of physical activity (as indicated by walking faster) will confer a greater benefit in diabetes risk reduction,
      • Gill J.M.
      • Cooper A.R.
      Physical activity and prevention of type 2 diabetes mellitus.
      which warrants further research.
      This study included a large number of participants, which provided a sufficient sample size for the analysis to be undertaken, particularly on the subgroup analysis by physical activity level. This provides novel insight into the association’s consistency across different physical activity levels. The measurement of walking pace is of low cost, is easy to administer, and would therefore be relatively simple to implement into clinical practice for risk prediction/stratification. The previous studies concluded that the age at diagnosis of T2D was early, particularly 40 years or younger.
      • Holden S.E.
      • Barnett A.H.
      • Peters J.R.
      • et al.
      The incidence of type 2 diabetes in the United Kingdom from 1991 to 2010.
      ,
      • Wang Z.
      • Wu Y.
      • Wu J.
      • et al.
      Trends in prevalence and incidence of type 2 diabetes among adults in Beijing, China, from 2008 to 2017.
      We found that in individuals who reported a slow walking pace, T2D will develop earlier than in those who had brisk walking pace. Therefore, assuming causality, brisk walking pace should be promoted among adults to reduce the risk for development of T2D. Although our study used self-reported usual walking pace, which may be more prone to self-reported bias, evidence suggests that self-reported walking pace is a strong predictor of health and a good proxy of gait speed.
      • Syddall H.E.
      • Westbury L.D.
      • Cooper C.
      • Sayer A.A.
      Self-reported walking speed: a useful marker of physical performance among community-dwelling older people?.
      However, our study has limitations. The UK Biobank is not representative of the general population of the United Kingdom, including sociodemographic, physical, lifestyle, and health-related characteristics of the general population. Although absolute risk would not be applicable to the general population, exposure-disease risk estimates should be generalizable.
      • Celis-Morales C.A.
      • Petermann F.
      • Hui L.
      • et al.
      Associations between diabetes and both cardiovascular disease and all-cause mortality are modified by grip strength: evidence from UK Biobank, a prospective population-based cohort study.
      ,
      • Fry A.
      • Littlejohns T.J.
      • Sudlow C.
      • et al.
      Comparison of sociodemographic and health-related characteristics of UK Biobank participants with those of the general population.
      The observational nature of the study does not allow us to infer causality; however, evidence from randomized controlled trials has shown beneficial effects of brisk walking on preventing T2D and improving glycemic control in people with diabetes.
      • Karstoft K.
      • Winding K.
      • Knudsen S.H.
      • et al.
      The effects of free-living interval-walking training on glycemic control, body composition, and physical fitness in type 2 diabetic patients: a randomized, controlled trial.
      Reverse causation may still be possible even though a 2-year landmark analysis was conducted and individuals with diabetes at baseline were excluded.

      Conclusion

      This study provides evidence that slow walking pace is associated with a higher incident T2D in both men and women, independent of key confounding factors, including adiposity and total physical activity. Self-reported walking pace may be a useful marker to identify people who are at high risk for development of T2D, which warrants further research.

      Potential Competing Interests

      The authors report no competing interests.

      Acknowledgments

      We are grateful to UK Biobank participants. This research has been conducted using the UK Biobank resource under application number 7155.
      Drs Ho, Gray, and Celis-Morales contributed equally and are joint senior authors.

      Supplemental Online Material

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      • In the Limelight: September 2022
        Mayo Clinic ProceedingsVol. 97Issue 9
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