Journal Logo

Clinical Sciences: Clinical Investigations

Effect of a rhinovirus-caused upper respiratory illness on pulmonary function test and exercise responses


Author Information
Medicine & Science in Sports & Exercise: May 1997 - Volume 29 - Issue 5 - p 604-609
  • Free


Viruses are the most common infectious agents affecting humans. Some investigators contend that viral upper respiratory illness (URI) causes more frequent acute disability among athletes than all other diseases combined(27). Disease patterns among summer and winter Olympic athletes are remarkably consistent, with respiratory infections heading the list followed by gastrointestinal disorders and skin infections(20). In the 1992 winter Olympics, some of the world's greatest athletes were unable to compete or did not perform strongly because of a URI (23), and several athletes were reportedly unable to compete in the 1988 summer Olympic games as a result of infectious illness (16). The average adult has from one to six colds each year (2,7) with human rhinoviruses (HRV) accounting for about 40% of these infections. Heavy exercise may enhance the risk of acquiring a URI (23). RV infections are most prevalent in the fall and spring months (11). In the United States, these infections are associated with major socio-economic expense, costing five billion dollars annually as a result of truancy from work and school, physician expenses, and over-the-counter medications(29). Athletes and exercise enthusiasts, however, commonly continue to participate in competitive and recreational sports during URI.

Unfortunately, little information is available related to physiological changes that may occur during exercise with a rhinovirus-caused URI. Detectable abnormalities in pulmonary functional capacity, such as forced expiratory volume and forced vital capacity, are known to occur during infectious illness, including URI (21,22,24). The authors of these studies conclude that weakness in the inspiratory muscles may contribute to breathlessness during exertion. Others(4,12,17,18) also add that this weakness may explain why athletic performance tends to be reduced during viral illness, suggesting that perhaps strenuous exercise should be avoided during such infections. Upper respiratory illness caused by rhinoviruses can produce transient peripheral airway abnormalities (8).

Alterations in muscle ultrastructure and enzyme activity have been identified during viral and mycoplasma infections (5). Roberts (26) suggests that a decrease in muscle glycogen utilization occurs during viral illness while Ardawi (3) reports that a decrease in muscle glutamine release occurs with URI during prolonged physical training. Coxsackie viruses can cause URIs but may also cause myocarditis or pericarditis, which may increase the risk of acute arrhythmias leading to sudden death (26). Because of these widespread pulmonary, cardiac, and skeletal muscle effects, it appears plausible that a URI may decrease exercise functional capacity.

However, many of the studies described above suffer from a common weakness. Various viral illnesses are lumped together as if they represent a homogeneous phenomenon, which they are not. For example, one study (5) lumps patients with such diverse infections as varicella, influenza, coxsackie B2, and Mycoplasma pneumoniae (a bacterium) into a single test group. Additionally, the studies described above all use viruses that produce viremias (virus in the blood) and infect a wide variety of host tissues. This contrasts starkly with rhinoviruses, which are restricted to the upper respiratory tract and produce no viremia because of their strict temperature optimum (33-35°C). Exercise performance effects seen with viremic infections may well be a result of invasion of skeletal muscle or heart tissue. In contrast, any rhinovirus effects on exercise performance must be restricted to those that emanate from invasion of the upper respiratory tract and localized production of kinins and interleukins. The purposes of this study were to determine the impact of a rhinovirus-caused URI on submaximal exercise responses, maximal exercise functional capacity, and resting pulmonary function.


Subjects. Student volunteers were solicited from classes in the School of Physical Education at Ball State University. An initial screening consisted of a health history questionnaire including information regarding acute and chronic diseases, asthma, bronchitis, chronic colds, allergies(including penicillin), pregnancy, immune deficiency, medications, and physical activity level. Volunteers were enrolled in the study only if they were judged to be healthy according to the criteria of the American College of Sports Medicine (1) and engaged in 3 d·wk-1 of physical activity (i.e., 30 min of aerobic activity). All subjects agreed to refrain from self treating their colds (e.g., no over-the-counter medications) during the initial 3 d of the URI. All subjects signed an informed consent form approved by the Institutional Review Board. Subjects who completed the study received modest remuneration for their efforts.

Following the initial health history screening, volunteers meeting the above criteria were serologically evaluated for the human rhinovirus type 16(HRV 16) antibody. Blood specimens were obtained and serum neutralizing antibody to HRV 16 were assayed in each specimen. Forty-five subjects (20 females, 50 males) who tested negative to the HRV 16 antibody were randomly assigned to the experimental group while 10 subjects (5 females, 5 males) were assigned to the control group. The physical characteristics are presented for both groups in Table 1. Subject groups did not differ in age, height, weight, or body fat. All of the experimental group subjects had an oral temperature below 100°F prior to testing.

Experimental design. All subjects completed both a baseline pulmonary function test and a graded exercise test to volitional fatigue. Experimental subjects were inoculated with HRV 16 on two consecutive days within 10 d of completing these tests. The day following the second inoculation (peak of illness), post-inoculation pulmonary function and graded exercise tests were again performed. A noninfected control group completed these same pulmonary and exercise tests 1 wk apart.

Virus detection and quantification (pre-inoculation). Just prior to HRV 16 inoculation, a pre-inoculation nasal wash was taken from all subjects. This pre-inoculation nasopharyngeal sample was used to detect most respiratory viruses that may be carried subclinically or in incubation by the subjects. Subjects with previous infections could then be eliminated from the experiment. Nasal wash samples were inoculated in cell cultures of human diploid cells, primary rhesus monkey kidney, and a continuous cell line, HEp-2. The diploid cells were incubated at 33°C on a slowly rolling drum, and the other two cell cultures in a stationary rack at 37°C. The cultures were examined by microscope approximately every other day, and standard techniques were used for detection and identification of viruses, e.g., hemadsorption for myxo- and paramyxoviruses, acid lability for rhinoviruses, etc. (13,15). These cell cultures could not detect all possible viruses (e.g., most coronavirus infections and many coxsackie A viruses).

Virus detection and quantification (post-inoculation). Beginning the day following infection (Day +2), nasal washings were again obtained, titrated in serial 10-fold dilutions and placed in human diploid cell cultures. Virus specimens were quantitated for HRV 16. Nasal washes were taken on two consecutive mornings following the second day of inoculation.

Inoculation and clinical evaluation of URI. As outlined by Dick(13,15), each subject was inoculated intranasally by aerosol, using an office atomizer, and by pipette with about 1,000 infectious particles of safety-tested HRV 16. This inoculation was repeated the next day (Day +2). Typically, the evening of Day +2 the subjects begin to have a slight sore throat, and symptoms become fully developed on Days +3 and+4. Often they diminish rapidly thereafter and the subjects are well within a week. The colds are very ordinary with nasal stuffiness, rhinorrhea, cough(usually after Day +3), and some malaise. About 1-2% will have a fever over 100°F.

Prior to infection, each subject filled out a previously validated symptom checklist (13-15). This activity was repeated prior to the inoculation on the second day and prior to the graded exercise testing on the third day. Subjects rated (0 = not present, 1 = mild, 2 = moderate, 3 = Severe) the severity of 13 common cold symptoms. A cold with a total score of less than 7 is considered mild; 7-11, moderate; 12 or greater, severe.

Pulmonary function testing. Measures of pulmonary function were made immediately prior to each exercise test using a Spiromate AS-600 (Riko Corp., Lake Success, NY) spirometer, which was calibrated using a 3-L syringe immediately prior to each testing session. Forced vital capacity (FVC), forced expiratory volume in 1 s (FEV1.0), and peak expiratory flow (PEF) were measured during three successive maneuvers of having the subject exhale as forcefully and rapidly as possible following a maximal inspiration. The highest value was selected for data analysis purpose. After a brief rest period, maximal voluntary ventilation (MVV) was also determined. Each subject was instructed to breath as deeply and rapidly as possible for 12 s. The volume obtained during this procedure was multiplied by 5 to obtain the MVV value.

Graded exercise testing.Body composition. Height and weight were measured using a standard physician's scale. Body density was estimated using skinfold measurements with Lange calipers according to the procedures outlined by Pollock et al. (25), and body fat was determined using the formula developed by Siri (28). The skinfold sites included the chest, abdomen, and thigh for the men, and the triceps, supraillium, and thigh for the women. Subjects were prepared for the exercise ECG using a CM-5 configuration, during which time the Borg rating of perceived exertion (RPE) scale (9) and instructions for the test were explained. The ECG was monitored continuously during the exercise test using a Physio-Control Lifepak 7 (Redmond, WA).

A Sensormedics 2900 Metabolic Measuring Cart (Yorba Linda, CA) was used for all metabolic measurements with a Hans Rudolph 2700 series one way non-rebreathing valve (Kansas City, MO) and mouthpiece. Breath-by-breath analysis of expired air was performed, and the data were expressed using a five breath average for each subject tested. The ventilatory threshold was calculated using the V-slope technique, a method for detecting anaerobic threshold by gas exchange (6).

Two standardized incremental treadmill protocols, one for men and one for women, were used in this study. Both protocols consisted of 1-min stages (one MET increments) and began with 5-6 min of graded walking and then progressed to running speeds. All subjects were encouraged to give a maximal effort and were provided with strong verbal prompts throughout the testing sessions. The exercise tests were terminated when the subjects indicated they could no longer maintain the speed/grade on the treadmill. All subject responses met the minimum standard of RER ≥ 1.1 and HRmax > (220-age-15 beats·min-1). Heart rate and RPE were recorded during the last 10 s of each stage.

Statistical analysis. Symptom severity scores from the Cold Symptom checklist were summed with subjects' colds categorized as either subclinical/mild (symptom score 7 or lower, N = 17; 13 males, 4 females), or moderate/severe (symptom score higher than 8, N = 28; 12 males, 16 females). A 3 × 2 ANOVA with repeated measures for all three groups (subclinical/mild, moderate/severe, and control group), for both trials (pre- and post-inoculation) was used to analyze both the maximal and submaximal exercise test data and the pulmonary function data. The criterion for statistical significance was P < 0.05.


Pulmonary function analysis. There was no significant interaction between treatment (pre/post URI) and group (control, mild, severe) for any of the pulmonary function measures obtained. There was a significant difference between groups in their FEV1.0/FVC measures with the severe group (84.2± 2.3%) being lower than the mild group (88.9 ± 2.6%) which in turn was lower than the control group (92.7 ± 2.2). It should be noted, however, that all of these values are within the normal range for this measurement. The only treatment difference observed was the MVV with the post-treatment measure being 12.9 ± 2.1 L·min-1 higher than the pretreatment condition for all groups combined. There were no significant differences observed for FVC, FEV1.0, or PEF.

Maximal graded exercise. Maximal values obtained for the control group and for the experimental group before and after inoculation with significant group by treatment interaction was found for ˙VO2 max. There was no difference in the pre/post ˙VO2max values for the control group; however, both the subclinical mild and moderate severe URI groups demonstrated small increases of 2.4 ± 0.8 and 3.8 ± 1.8 mL·kg-1·min-1 in their post inoculation test(Table 2). Although ˙VEmax was significantly higher in subclinical mild group and RER was significantly lower in the post-inoculation test, there were no significant group by treatment interactions for these or any of the other variables assessed.

Submaximal graded exercise. Submaximal values obtained before and after inoculation for all three groups are presented inTables 3 and 4 at all three time periods (2, 5, and 8 min). There was no difference in the post-test ˙VO2 for the subclinical mild and moderate severe URI groups; however, the control group had small, yet statistically significant, increases of 1.4 ± 0.7 and 1.6 ± 0.6 mL·kg-1·min-1 at the 2- and 5-min time periods, respectively. There were no significant group by treatment effects or treatment by group interactions for any of the other variables assessed. Additionally, there were no significant group, treatment, or interactive effects for ventilatory threshold (VT) or HR VT (seeTable 5).


A surprising finding from this investigation was the lack of any significant impairment in any of the measures of pulmonary function in those who were inoculated with HRV 16 (Table 6). Although data are sparse, it has been suggested that forced expiratory volume and forced vital capacity are lower in young adults during viral (influenza A) infection(8). Other research suggests that HRV 13 and HRV 15 can produce transient peripheral airway abnormalities (21). Two factors could be considered here. At least for the first investigation mentioned above, one can expect greater morbidity from the influenza A virus and likely subsequent inability to perform exercise. The other factor to consider is that pulmonary function tests principally measure large airway responses. It may be possible that smaller airways demonstrate abnormalities in the infected state.

The most noteworthy finding of this investigation was the lack of any significant impairment in ˙VO2max in those who were inoculated with a rhinovirus. Surprisingly, when compared with the control group, both illness severity groups had slightly higher ˙VO2max values when tested after being inoculated compared with the pre-inoculation test. Although this finding was statistically significant, the practical significance is questionable. The explanation for the higher ˙VO2max in those with symptoms of a URI is not readily apparent. It is possible that the increase observed on the second test was a learning effect; however, the control group did not show evidence of this same learning effect. From a technical viewpoint, all of the subjects tested reached the preset criteria for˙VO2max, and all were given substantial verbal encouragement to provide a maximal effort. Other physiological markers measured at maximal effort (HR, ˙VE, RER, RPE) also showed no significant interactions between subject groups and treatment. Finally, it should be noted that the coefficient of variation for ˙VO2max measures has been reported to range from 3.2 to 4.4%, (10,19) which suggests that the difference observed may be a result of measurement variability between repeated tests. Perhaps psychological effects (e.g., anxiety) caused the subjects to exert more effort during their post-inoculation tests. Also, there may have been an order effect by the subjects completing their baseline tests prior to completing their post-inoculation tests. Maybe the results would have been different if subjects had completed post-inoculation tests prior to completing their baseline tests.

Similar to the findings associated with the maximal responses, there was a lack of significant impairment in any of the markers of submaximal exercise response in those who were inoculated with a rhinovirus. Again, this finding was consistent among those with subclinical/mild symptoms and those with moderate and severe symptoms and spanned exercise intensities of approximately 32, 50, and 70% of ˙VO2max. Interestingly, although subjects inoculated with HRV 16 reported symptoms such as nasal discharge, aching joints/muscles, and sore throat, they did not perceive the exercise effort to be more difficult at equivalent time periods during the exercise test.

Although this study did not compare steady state exercise responses, the available data would suggest that athletes or exercisers need not modify exercise intensity during a URI. Further support for this comes from the finding of no difference in ventilatory threshold during a URI. Whether the frequency and/or duration of exercise training sessions would need to be modified for those with URI cannot be addressed with these data.


This investigation indicated that a rhinovirus-caused URI does not affect resting pulmonary function or limit one's capability to perform acute submaximal or acute maximal bouts of exercise on a treadmill. However, this is the first study to examine the affect of a URI of known etiology on physiological responses to exercise. Perhaps changes in physiological responses during exercise with a rhinovirus-caused URI may be seen during longer submaximal exercise bouts as opposed to acute maximal bouts of exercise. For example, in a submaximal exercise bout of 45 min, could a rhinovirus-caused URI impact performance? Finally, this study was limited to a young population. We recommend that future studies be conducted on various age groups to determine if age is a factor in physiological responses to exercise during a rhinovirus-caused URI.



1. American College Of Sports Medicine. Guidelines for Exercise Testing and Prescription, 4th ed. Philadelphia: Lea and Febiger, 1991, pp. 3-10.
2. Andrews, C. The Common Cold. New York: W.W. Norton and Company, Inc., 1965, pp. 13-107.
3. Ardawi M. S. and E. A. Newsholme. Metabolism in lymphocytes and its importance in the immune response. Essays Biochem 21:1, 1985.
4. Assmussen, E. and B. Mazin. A central nervous component in local muscular fatigue. Eur. J. Appl. Physiol. 38:9-15, 1978.
5. Astrom, E., G. Friman., and L. Pilstrom. Effects of viral and mycoplasma infections on ultrastructure and enzyme activities in human skeletal muscle. Acta Path. Microbiol. Scand. Sect. A. 84:113-122, 1976.
6. Beaver, W. L., K. Wasserman, and B. J. Whipp. J. A new method for detecting the anaerobicc threshold by gas exchange. Appl. Physiol. 60:2020-2027, 1986.
7. Beneson A. S. Acute Viral Respiratory Disease in Control of Communicable Diseases in Man. Washington: American Public Health Association, 1975, pp. 262-266.
8. Blair, H., S. Greenberg, P. Stevens, P. Bilunos, and R. Couch. Effects of rhinovirus infection on pulmonary function of healthy human volunteers. Am. Rev. Respir. Dis. 114:95-102, 1976.
9. Borg, G. Perceived exertion: a note on the“history” and methods. Med. Sci. Sports 5:90-93, 1973.
10. Bruce, R. A., F. Kusumi, and D. Hosmer. Maximal oxygen intake and nomographic assessment of functional aerobic impairment in cardiovascular disease. Am. Heart J. 85:546-562, 1973.
11. Casey J. M. and E. C. Dick. Acute respiratory infections. In: Winter Sports Medicine, J. M. Casey, C. Foster, and E. G. Hixson (Eds.). Philadelphia: F. A. Davis Co., 1990, pp. 112-128.
12. Daniels, W., D. Sharp, J. Wright, et al. Effects of virus infection on physical performance in man. Military Med. 150:8-14, 1985.
13. Dick, E. C., S. U. Hossain, K. A. Mink, et al. Interruption of transmission of rhinoviral colds among human volunteers using a virucidal facial tissue. J. Infect. Dis. 153:352-356, 1986.
14. Dick, E. C. and S. L. Inhorn. Rhinoviruses. In:Textbook of Pediatric Infectious Diseases, 3rd Ed. R. D. Geigin and J. D. Cherry (Eds.). Philadelphia: W. B. Saunders Co., 1992, pp. 1507-32.
15. Dick, E. C., L. C. Jennings, K. A. Mink, C. D. Wartgow, and S. L. Inhorn. Aerosol transmission of rhinovirus colds. J. Infect. Dis. 156:442-448, 1987.
16. Fitzgerald, L. Exercise and the immune system.Immunol. Today 9:337, 1988.
17. Friman, G. Effect of acute infectious disease on isometric muscle strength. Scand. J. Clin. Lab. Invest. 37:303-308, 1977.
18. Friman, G., J. Wright, N. Ilback, et al. Does fever or myalgia indicate reduced physical performance capacity in viral infections?Acta Med. Scand. 217:353-361, 1985.
19. Froelicher, V. F., H. Brammell, G. Davis, I. Noguera, A. Stewart, and M. C. Lancaster. A comparison of three maximal treadmill exercise protocols. J. Appl. Physiol. 36:720-725, 1974.
20. Hanley, D. F. Medical care of the US Olympic team.JAMA 236:147, 1976.
21. Little, J., W. Hall, G. Douglas, R. Hyde, and D. Speers. Amantidine effect on peripheral airway abnormalities in influenza. Ann. Intern. Med. 85:177-82, 1976.
22. Mier-Jedrzejowicz, A., C. Brophy, and M. Green. Respiratory muscle weakness during upper respiratory tract infections.Am. Rev. Respir. Dis. 138:5-7, 1988.
23. Nieman, D. C. Exercise, immunity and respiratory infections. Sport Sci. Exchange 4:39, 1992.
24. O'Connor, S., P. Deric, J. Collins, et al. Changes in pulmonary function after naturally acquired respiratory infection in normal persons. Am. Rev. Respir. Dis. 120:1087-1093, 1979.
25. Pollock, M., D. Schmidt, and A. Jackson. Measurement of cardiorespiratory fitness and body composition in the clinical setting.Compr. Ther. 6:12-27, 1980.
26. Roberts, J. A. Viral illnesses and sports performance.Sports Med. 3:296-303, 1986.
27. Ryan, A. J., W. Dalrymple, B. Dull, W. S. Kaden, and S. J. Lerman. Round table: Upper respiratory infections in sports.Physician Sportsmed. 3:29-42, 1975.
28. Siri, W. E. Body composition from fluid spaces and density. Med. Phys. Rep. March, 1956.
29. Turner, R. The role of neutrophils in the pathogenesis of rhinovirus infections. J. Pediatr. Infect. Dis. 9:838-835, 1990.
30. Verde, T., S. Thomas, R. Moore, P. Shek, and J. Shephard. Immune responses and increased training of the elite athlete.J. Appl. Physiol. 73:1494-1499, 1992.


©1997The American College of Sports Medicine