Immune Response to a 30-Minute Walk

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Immune Response to a 30-Minute WalkDAVID C. NIEMAN, DR U A. HENSON, MELANIE D. AUSTIN, and VICTOR A. BROWNDepartmentof Health, Leisure, and Exercise Science; AppalachianState University, Boone, NC

ABSTRACTNIEMAN, D. C., D. A. HENSON, M. D. AUSTIN, ans V. A. BROWN. Immune Response to a 30-Minute Walk. Med. Sci. SportsExerc., Vol. 37, No. 1,pp. 5 7 -62, 2005. Purpose: To measure several components of immune changes related to walking 30 min withor without an exercise assist device compared with sitting. Methods: Fifteen healthy and nonobese female subjects (37.5 3:1 yr ofage) accustomed to regular walking were recruited and tested for aerobic power (VO,. 34.4 1.4 mL-kgi'-min-'). During threerandomly assigned 30-min test sessions, subjects functioned as their own controls and either sat in the laboratory, walked at -60%VO2m-, or walked at the same treadmill speed using the BODY BAT3 Aerobic Exerciser. This exercise assist device resembles a pairof baseball bats seamlessly joined together and is held with both hands and swung to shoulder height across the body in a natural sideto side pendulum motion. Saliva and blood samples were collected pre- and postexercise, and I h postexercise, with the data statisticallyanalyzed using a 3 x 3 repeated measures ANOVA. Results: Walking with the exercise assist device increased oxygen consumptionII 2% and heart rate 8 2 beats-min- '.The pattern of increase in blood counts for neutrophils, lymphocytes, monocytes. and natural

killer cells, plasma interleukin-6 concentration, and PHA-induced lymphocyte proliferation differed significantly when comparingwalking with sitting, but no differences were found between walking with or without the exercise assist device. No significant increasesover time or interaction effects were measured for plasma cortisol concentration, salivary IgA output, or plasma interleukin- I receptorantagonist concentration. Conclusions: The use of an exercise assist device increased oxygen consumption 11% during walking, butdid not alter the pattern of change in several components of immunity measured during walking alone in comparison to sitting. Walkingcaused modest and short-lived changes in immune parameters, most notably for neutrophil and natural killer blood cell counts. KeyWords: IMMUNE FUNCTION, NEUTROPHILS, NATURAL KILLER CELLS. T-CELL FUNCTION, SALIVARY IgA

P eople who exercise regularly report fewer upper re-spiratory tract infections (URTI) than their sedentarypeers (12). Data from three randomized studies sup-

port this viewpoint that near-daily physical activity reducesthe number of days with sickness (14,19,20). In these stud-ies, women in the exercise groups walked briskly 35-45min, 5 d.wk-1, for 12-15 wk during the winter/spring orfall, while the control groups remained physically inactive.Walkers experienced about half the days with URTI symp-toms of the sedentary controls. Epidemiologic research alsosupports a reduction in URTI risk for those engaging inregular versus irregular moderate-to-vigorous physical ac-tivity (7), in contrast to an elevated URTI risk in athletestraining heavily or competing in marathon race events (16).

The exercise link with lowered URTI risk suggests thatpositive immune changes occur during physical activity. Incontrast to animal studies (3,6), randomized exercise train-ing human studies have failed to demonstrate that immune

Address for correspondence: David C. Nieman, Department of Health,Leisure. and Exercise Science, Appalachian State University. P.O. Box32071, III Rivers Street, Holmes Convocation Center, Boone, NC 28608;E-mail: [email protected] for publication July 2004.Accepted for publication August 2004.0195-9131/05/3701-0057MEDICINE & SCIENCE IN SPORTS & EXERCISE,Copyright g 005 by the American College of Sports MedicineDOI: 10.1249/01.MSS.0000149808.38194.21

function measured in the resting state is altered after 12-15wk of near-daily moderate physical activity (14,19,20). Forthese reasons, we have hypothesized that the acute immunechanges occurring during and shortly after the moderateexercise bout itself may explain the lowered risk of URTI(12). In other words, host protection against pathogens isimproved through a summation effect of improved immu-nosurveillance that occurs acutely with each moderate ex-ercise bout. This link, however, has not yet been establishedand will require periodic immune testing before and afterwalking in a large cohort of individuals randomized tomoderate exercise and sedentary groups and followed forURTI incidence.

In comparison with high-intensity, long-duration exercise(10,11,15), a dearth of published information exists on theacute immune response to 30 min of brisk walking (or similaractivity), a commonly prescribed exercise (12,17,18). Severalstudies suggest positive immune changes during moderate ac-tivity (8,9,18,20), but only a few different types of immunemeasures have been conducted, and a resting control conditionhas often been lacking. Exercise assist devices such as walkingpoles or hand weights are often used by walkers (13), but noinformation exists regarding the effect of using exercise assistdevices on immune responses to walking. The purpose of thisstudy was to a measure a wide range of immune changes inresponse to walking for 30 min with or without an exerciseassist device compared with sitting in female subjects accus-tomed to walking. We hypothesized that walking with theexercise assist device would increase perturbations in severalcomponents of immunity measured during walking alone.


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METHODSSubjects. Fifteen female subjects between the ages of20 and 55 were recruited. Recruitment into the study wascontingent upon several characteristics: body mass index(BMI) of less than 35 kg-m- 2 , healthy (with no knowndisease or medication use), and accustomed to walking(history of walking at least 20-30 min, 2-7X wk-', for theprevious 3 months or longer). Informed consent was ob-tained from each subject, and the experimental procedureswere in accordance with the policy statements of the insti-tutional review board of Appalachian State University.Research'design. In the first test session, subjectsfilled out a medical/health questionnaire and were tested forbody composition and maximal aerobic fitness. Maximalaerobic power (VO2max) and other metabolic measures weredetermined during the Bruce graded maximal treadmill pro-tocol with the MedGraphics CPX Express metabolic system(MedGraphics Corporation, St. Paul, MN) (2). Submaximaland maximal heart rates were measured using a chest heartrate monitor (Polar Electro Inc., Woodbury, NY). VO2n,axwas achieved when subjects achieved two of three criteria:respiratory exchange ratio (RER) -1.1, oxygen consump-tion increased


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PH A was prepared in RPMI-1640 media, at a concentrationof I mg.mL- , and then further diluted with complete mediato the optimal and suboptimal working concentrations (12Ag-mL-' and 6 ,uggmL-, respectively). A 100-,LL aliquotof the diluted blood was dispensed into each of triplicatewells of a 96-well flat-bottom microtiter plate. To each well,100 ,uL of the appropriate.mitogen dose was added. Controlwells received complete media instead of mitogen. After a72-h incubation at 37 0C and 5% C0 2 , the cells were pulsedwith I ,uCi of thymidine (methyl)- 3 H (New England Nu-clear, Boston, MA) prepared with RPMI-1640. After puls-ing, cells were incubated for an additional 4 h before har-vesting. The radionucleotide incorporation was assessed byliquid scintillation counting with the results expressed asexperimental minus control counts per minute (cpm). Theintraassay CV was less than 10%. PHA-induced prolifera-tion expressed on a "per T-cell" basis was calculated bydividing the cpm data by the number of T-cells in the assaywells.Cytokine measurements. Total plasma concentra-tions of interleukin-l receptor antagonist (IL-lra) and inter-leukin-6 (IL-6) were determined using quantitative sand-wich ELISA kits provided by R& D Systems, Inc.(Minneapolis, MN). All samples and provided standardswere analyzed in duplicate. A standard curve was con-structed using standards provided in the kits, and the cyto-kine concentrations were determined from the standardcurves using linear regression analysis. The assays were atwo-step "sandwich" enzyme immunoassay in which sam-ples and standards were incubated in a 96-well microtiterplate coated with polyclonal antibodies for the test cytokineas the capture antibody. After the appropriate incubationtime, the wells were washed, and a second detection anti-body conjugated to either alkaline phosphatase (IL-6 highsensitivity) or horseradish peroxidase (IL-Ira) was added.The plates were incubated and washed, and the amount ofbound enzyme-labeled detection antibody was measured byadding a chromogenic substrate. The plates were then readat the appropriate wavelength. The minimum detectableconcentration was


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TABLE 3. Change in leukocyte subset counts during sitting and walking with orwithout an exercise assist device.Sit Walk BODY BATPreexercise Preexercise PreexercisePostexercise Postexercise Postexercise PVariable 1-h 1-h 1-h Interaction;

(109 L-1) postexercise postexercise postexercise TimeNeutrophils 4.03 0.43 3.79 0.28 3.52 + 0.29 0.048;


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* Sittng3-

2.5 -

2 -

-J 1.5 -rCDIj 1 A4

TABLE 4. Salivary IgA during sitting and walking with or without an exerciseassist device.Sit Walk BODY BATPreexercise Preexercise PreexercisePostexercise Postexercise Postexercise P1-h 1-h 1-h Interaction;Variable poslexercise postexercise postexercise Time

sigA concentration 32 9 30 329 + 25 322 29 0.686; 0.113(gg.mL- 1) 34 9 + 32 333 29 347 +27341 28 36 6 31 371 33Saliva volume 2.97 + 0.27 2.96 0.17 2.94 + 0.22 0.764; 0.159(mL.4 min-') 2.90 + 0.24 2.84 0.30 2.63 + 0.182.91 + 0.25 2.63 + 0.25 2.61 0.24sigA secretion rate 22 7 + 20 238 + 22 225 + 22 0.93; 0.987(Sggmin-') 23 8 + 22 222 + 4 224 + 24232 18 22 6 21 22 9 20sIgA:protein 42 0 + 41 433 + 43 44 9 + 31 0.300; 0.006(Gg.mg-') 41 6 + 39 361 + 45 33 8 40434 43 40 6 +27 46 6 42

Pre-Exercise

o.sI

ao

T TI

lymphocyte proliferation at a mitogen concentration of and 6,ag-mL-l (P = 0.107) (data not shown).

No significant time or interaction effects were measuredfor salivary IgA concentration or secretion rate (Table 4) orIL-Ira (Table 5). Plasma cortisol concentration droppedover time for all three conditions, and the pattern of decreasedid not differ between conditions (interaction effect, P =0.797) (Table 5). The pattern of increase in plasma IL-6concentration differed significantly when comparing walk-ing with sitting, but no differences were found betweenwalking with or without the exercise assist device (Fig. 4)(time and interaction effects, P < 0.001 and P = 0.008,respectively).

DISCUSSIONThese data indicate that the use of an exercise assist

device increased oxygen consumption 11% during walkingbut did not alter the pattern of change in several componentsof immunity measured during walking alone in comparisonwith sitting. Walking for 30 min at 60-65% VOmax with orwithout an exercise device compared with sitting causedmodest and short-lived increases in several leukocyte sub-sets, primarily neutrophils, and natural killer cells. Mitogen-induced lymphocyte proliferation was elevated immediatelyafter walking compared with sitting, but this increase wasdue to the influx of T lymphocytes into the blood compart-ment. No increase in the plasma concentration of the anti-inflammatory cytokine IL-Ira wa s measured during walkingcompared with sitting, and plasma IL-6 concentration wasTABLE 5.Plasma cortisol and IL-lra during sitting and walking with or without anexercise assist device.

Sit Walk BODY BA TPreexercise Preexercise PreexercisePostexercise Poslexercise Postexercise R1-h 1-h 1-h Interaction;Variable postexercise postexercise postexercise TimeCortisol (nmol.L-1) 186 33 236 t 35 208 + 25 0.797; 0.026166 20 249 61 187 20136+14 187+33 1879IL-lra (pg.mL-') 168 + 26 178 + 34 159 18 0.292; 0.102175+26 213+37 163+16

17125 18934 168+17P< 0.01, increase greater compared with sitting condition.

FIGURE 4-The pattern of increase in IL-6 differed significantlywhen comparing walking with sitting, but no differences were foundbetween walking with or without the exercise assist device. Time andinteraction effects, P < 0.001 an d P = 0.008, respectively). **P < 0.01increase greater compared to sitting condition.

increased slightly but significantly. Walking did not causean increase in cortisol. Subjects in our study were trainedwalkers, and these data may not be applicable to sedentaryindividuals.Walking briskly with the exercise device only increasedoxygen consumption 11%, and this was not enough to altethe immune response. In a previous study, we showed thawhen walking 4.0 and 4.8 km h- , use of the BODY BA Tincreased the heart rate by about 20 beats-min-', and aug-mented oxygen consumption 32-42% (13). In the presentstudy, subjects walked more briskly (- 6.3 km h-1), andthis resulted in a smaller metabolic difference betweenwalking with or without the BODY BAT.

In contrast to moderate exercise such as 30 min of briskwalking, intense and prolonged exertion causes large in-creases in blood leukocyte, neutrophils, and monocytescounts, plasma cortisol concentration, plasma IL-6 and IL-lra concentrations, and large postexercise decreases in sIgAsecretion rate, natural killer cell counts and activity, andPHA-induced lymphocyte proliferation (10,11,15). Theseimmune changes, measured after heavy exertion, have generally been interpreted as immunosuppressive, but a linkwith increased URTI risk has not yet been consistentlyestablished (10,1 1).

In the same way, the mild and transient immune pertur-bations measured after walking have been described asbeneficial to immunosurveillance (3,6,8,9,18,21), bu t a linkwith decreased URTI risk has not yet been measured, andthis was not the aim of the present study. Some data suggesthat the benefits of moderate exercise on immunity may berelated just as much to the absence of negative changes (e.g.large increases in stress hormones, cytokines, and apoptosis)as to improved immune recirculation. For example, Moorenet al. (8) showed that lymphocyte apoptosis occurs afteintensive and exhaustive exercise but not during moderateintensity exercise.

* Walking BODY BAT

**

*T*

Post-Exernise 1-h Post-Exercise


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The acute immune changes after moderate compared withintensive and prolonged exercise are widely disparate, andfurther research is warranted to deterniine whether or not URTIrisk can be linked to exercise workload in humans. In mnice,Davis et al. (3) has shown that I h of moderate exercise per dayfor 6 d in a row improved macrophage resistance to herpessimplex virus type 1 and reduced URTI risk.In summary, walking with or without an exercise assistdevice at 60-65% VO2max compared with sitting was as-sociated with modest and transient changes in blood cellcounts (especially neutrophils and natural killer cells),PHA-induced lymphocyte proliferation, and plasma IL-6

REFERENCESI. BRADFORD, M. M. A rapid and sensitive method for the quantita-

tion of microgram quantities protein utilizing the principle ofprotein-dye binding. Anal. Biochemn. 72:248-254, 1976.

2. BRUCE, R. A, F. KUSUMI, and D. HOSMER. Maximal oxygen intakeand nomographic assessment of functional aerobic impairment incardiovascular disease. Am . HeartJ. 85:546-562, 1973.

3. DAVIS, J. M., E. A. MuRPHY, A. S. BROWN, M. D. CARMICHAEL, A.GHAFFAR, and E. P. MAYER. Effects of moderate exercise and oat beta-glucan on innate immune function and susceptibility to respiratory in-fection. Ain. J. Physiol. Regul. Integr. Comp. Physiol. 286:R366-R372,2004.4. DILL, D. B., and D. L. COSTILL. Calculation of percentage changesin volumes of blood, plasma, an d red cells in dehydration. J. Appl.Physiol. 37:247-248, 1974.

5. JACKSON, A. S., M. L. POLLOCK, and A. WARD. Generalized equa-tions for predicting body density of women. Med. Sci. SportsExerc. 12:175-182, 1980.6. KOHUT, M. L., G. W. BOEHM, and J. A. MOYNIHAN. Moderateexercise is associated with enhanced antigen-specific cytokine, bu tnot IgM antibody production in aged mice. Mech. Ageing Dev.122:1135-1150, 2001.

7. MATTHEWS, C. E., l. S. OCKENE, P. S. FREEDSON, M. C. ROSAL, P. A.MERRIAM, and J. R. HEBERT. Moderate to vigorous physical activityand risk of upper-respiratory tract infection. Med. Sci. SportsExerc. 34:1242-1248. 2002.

8. MOOREN, F. C., D. BLOMING, A. LECHTERMANN, M. M. LERCH, andK. VOLKER. Lymphocyte apoptosis after exhaustive an d moderateexercise. J. Appl. Physiol. 93:147-153, 2002.9. NEHLSEN-CANNARELLA, S. L., D. C. NIEMAN, J. JESSEN, et al. Th eeffects of acute moderate exercise on lymphocyte function andserum immunoglobulins. Int. J. Sports Med. 12:391-398, 1991.

10. NIEMAN, D. C. Endurance exercise and the immune response. In:Enduranice in Sport, 2nd Ed., R. J. Shephard and P.-O. Astrand.Oxford, UK : Blackwell Science, 2000, pp . 731-746.

concentration, and no changes in plasma cortisol concen-tration, salivary IgA output, or plasma IL-Ira concentra-tion. These changes contrast sharply with the much largerperturbations we have reported following prolonged andintensive exercise such as marathon running (10,11,15).Further research is warranted to establish a link betweenthe acute immune changes occurring during each walkingbout with improved host protection against pathogens andlowered URTI risk.

This study was funded by a grant from Body Bat, Inc., P.O. Box66720, St. Petersburg, FL 33736-6720.

11. NIEMAN, D. C. Exercise effects on systemic immunity. Immunol.Cell Biol. 78:496-501, 2000.

12. NIEMAN, D. C. Is infection risk linked to exercise workload? Med.Sci. Sports Exerc. 32(Suppl. 7):S406-S411, 2000.

13. NIEMAN, D. C., and M. D. AUSTIN. The energy cost of using anexercise assist device during walking. Res. SportMed. 11:99-107,2003.

14. NIEMAN, D. C. , D. A. HENSON, G. GusEwrrcH, et al. Physicalactivity and immune function in elderly women. Med. Sci. SportsExerc. 25:823-831, 1993.

15. NIEMAN, D. C., D. A. HENSON, L. L. SMITH, et al. Cytokine changesafter a marathon race. J. Appl. Physiol. 91:109-114, 2001.

16. NIEMAN, D. C., L. M. JOHANSSEN, J. W. LEE, J. CERMAK, and K.ARABATZIS. Infectious episodes in runners before and after the Lo sAngeles Marathon. J. Sports Med. Phys. Fitness 30:316-328,1990.

17. NIEMAN, D. C., and S. L. NEHLSEN-CANNARELLA. The immuneresponse to exercise. Sem. Hematol. 31:166-179, 1994.

18. NIEMAN, D. C., S. L. NEHLSEN-CANNARELLA, K. M. DONOHUE, etal. The effects of acute moderate exercise on leukocyte an dlymphocyte subpopulations. Med. Sci. Sports Exerc. 23:578-585, 1991.

19. NIEMAN, D. C. , S. L. NEHLSEN-CANNARELLA, D. A. HENSON, et al.Immune response to exercise training and/or energy restriction inobese females. Med. Sci. Sports Exerc. 30:679-686, 1998.

20 . NIEMAN, D. C., S. L. NEHLSEN-CANNARELLA, P. A. MARKOFF, et al.The effects of moderate exercise training on natural killer cells andacute upper respiratory tract infections. Int. J. Sports Med. I 1:467-473, 1990.

21. ORTEGA, E., M. E. COLLAZOS, M. MAYNAR, C. BARRIGA, and M. DELA FUENTE. Stimulation of the phagocytic function of neutrophilsin sedentary men after acute moderate exercise. Eur. J. Appl.PhysioL 66:60-64, 1993.


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TITLE: Immune Response to a 30-Minute Walk

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