Journal List > J Korean Med Sci > v.37(14) > 1160642

Jeong, Oh, Lee, Lee, and Lee: Comparison of Predicted Exercise Capacity Equations in Adult Korean Subjects

Abstract

Background

Maximal oxygen uptake (VO2 max) is a useful index to assess exercise capacity. However, there is no reference value for Koreans. This study aimed to compare actual VO2 max and predicted VO2 max using exercise capacity equations in Korean subjects.

Methods

This retrospective study enrolled 383 patients who underwent cardiopulmonary exercise test (CPET) with incremental maximal cycle ergometer test at Asan Medical Center from January 2020 to May 2021. Stage 1 and 2 lung cancer patients with normal lung function and healthy persons of 50 subjects who had maximal CPET were analyzed.

Results

The subjects were aged 65 ± 13 years and predominantly male (74%). CPET results were as follows: absolute VO2 max, 1.2 ± 0.3 L/min; body weight referenced VO2 max, 20 ± 3.9 mL/kg/min; peak work rate, 94 ± 24 watts; peak heart rate, 142 ± 21 bpm; peak O2 pulse, 10 ± 3 mL/beat; minute ventilation, 59 ± 14 L/min; peak respiratory rate, 34 ± 6 breaths per minute; and peak breathing reserve, 41 ± 18%. There was significant discordance between the measured and predicted absolute VO2 max using the Jones, Hansen, and Wasserman prediction equations developed for Caucasian population (P < 0.001). Agreement using Bland-Altman test between true and predicted absolute VO2 max was the best in Chinese equation (−0.03, 2SD = 0.55) compared to Jones (0.42, 2SD = 1.07), Hansen (0.44, 2SD = 0.86), and Wasserman (0.42, 2SD = 0.86) equations.

Conclusion

The reference value and prediction equation from studies including primarily Caucasians may not be appropriate for Koreans. Since the mean difference is the lowest in Chinese equation, the Chinese equation might be used for the Korean adult population.

Graphical Abstract

jkms-37-e113-abf001.jpg

INTRODUCTION

Cardiopulmonary exercise test (CPET) is a widely used tool to evaluate the physiological response associated with cardiopulmonary disease, and its clinical usefulness has recently been demonstrated in respiratory diseases.1 Physiological responses of metabolic, cardiovascular, and ventilation systems that affect exercise ability can be evaluated by CPET, thus aiding in the diagnosis and treatment of patients. CPET is useful in the evaluation of the therapeutic effect and prognosis of respiratory diseases and in the diagnosis of dyspnea with unknown cause.
Maximal oxygen uptake (VO2 max) is a useful index for the assessment of exercise capacity, as it can powerfully predict outcomes of cardiac and pulmonary disorders.234567 VO2 max can be directly measured by CPET. Exercise capacity indicated by VO2 max can help in estimating cardiopulmonary risk, thus making the selection of normal reference value essential for interpretation.8
Different race and countries have various reference values due to the influence of factors such as age, sex, physical activity, and ethnicity.9 The American Thoracic Society/American College of Chest Physicians (ATS/ACCP) recommends selecting proper reference value that reflects the characteristics of the population. Most reference values and prediction equations are available for the Caucasians only.10111213 In contrast, there are few reference values for the Asians141516 and no reference value of VO2 max for Koreans. There are no reliable exercise capacity equations for VO2 max applicable to Koreans. We therefore compared measured VO2 max and predicted VO2 max using exercise capacity equations.

METHODS

Study subjects

This retrospective study was performed between January 2020 and May 2021, including 383 patients who underwent CPET with incremental maximal cycle ergometer test at Asan Medical Center, a 2,700-bed tertiary care center in Korea. The study group primarily consisted of patients being evaluated for pre-operative risk of lung cancer or dyspnea. Of these 383 patients, we selected 29 stage 1 and 2 lung cancer patients with normal lung and cardiac function and 21 healthy subject who had maximal CPET (Fig. 1). Healthy subjects were tested for unexplained dyspnea, but had no underlying medical conditions and no abnormal findings on chest X-ray, electrocardiograph (ECG), spirometry, and CPET. Maximal CPET was defined as the fulfillment of at least one of the following conditions: 1) Patients reached predicted VO2 max (> 85% predicted), 2) patients achieved predicted maximal heart rate (> 90% predicted), 3) patients had evidence of ventilatory limitation (breathing reserve < 20%), or 4) patients exhaustion was observed (Borg scale rating 9–10). The exclusion criteria were as follows: (1) patients who had sub-maximal CPET; and (2) patients who had lung resection surgery. The physical activity extent was graded according to international physical activity questionnaire.17
Fig. 1

The study flowchart.

CPET = cardiopulmonary exercise test, COPD = chronic obstructive pulmonary disease, COVID-19 = coronavirus disease 2019, PFT = pulmonary function test.
jkms-37-e113-g001

CPET protocol

CPET were performed on graded exercise using incremental protocol with cycle ergometer (VIAsprint 150P; Carefusion, San Diego, CA, USA),12 under physician’s supervision with defined criteria for termination: ischemic ECG changes, fall in systolic pressure > 20 from peak during test, and severe desaturation. CPET had four stages: resting, warm-up, exercise, and recovery stage. In the resting stage, subjects rested for 2 minutes before the test. In the warm-up stage, we collected sufficient baseline data such as oxygen saturation, heart rate, blood pressures, ECG, and expired gas analysis. Subject performed unloaded pedaling at 30–40 rpm for 1 minute and 30 seconds. In the exercise stage, considering general condition or pulmonary function results, subjects performed maximal exercise with pedaling at 60 rpm while increasing the load to 5–15 watts/min. During exercise, Borg dyspnea scale was recorded for all subjects. The test was stopped on the subject’s wishes or in case of an abnormal finding in medical monitoring. If the subject requested discontinuation of the test, the subject proceeds to the recovery stage. Finally, in the recovery stage, the subjects performed unloaded pedaling at 30–40 rpm for 2 minutes and we acquired physiologic data such as oxygen saturation, heart rate, blood pressures, and expired gas analysis until subject’s heart rate is stable.

Predicted exercise capacity equations

VO2 max was recalculated using different prediction equations. A detailed information of prediction equations is presented in Table 1.
Table 1

Main characteristics of predicted exercise capacity equations

jkms-37-e113-i001
Authors (year) Sample size (M/F) Age, yr Ethnic group Equipment Ref.
Jones et al. (1989) 50 M/50 F 15–71 Canadian Cycle 10
Hansen et al. (1994) 77 M 34–74 American Cycle 11
Wasserman (1999) 77 M 34–74 American Cycle 12
Dun et al. (2021) 558 M/406 F 18–70 Chinese Cycle 14
Jones et al.10a
VO2 (L/min) = 0.046 × Height − 0.021 × Age − 0.62 × Sex − 4.31
Hansen et al.11b
Male: VO2 (L/min) = Weight × [50.75 − (0.37 × Age)]/1,000
Female: VO2 (L/min) = (Weight + 43) × [22.78 − (0.17 × Age)]/1,000
Wasserman12c
Male: VO2 (L/min) = Weight × [50.72 − (0.372 × Age)]/1,000
Female: VO2 (L/min) = (Weight + 42.8) × [22.78 − (0.17 × age)]/1,000
Dun et al.14d
VO2 (L/min) = (1,532.58 – 328.244 × Sex – 9.951 × Age + 11.593 × Weight)/1,000
aSex, male = 0, female = 1; age, years; height, centimeters.
b,cAge, years; Weight, kilograms. Predicted weight men: 0.78 × Height (cm) − 60.7, Predicted weight women: 0.65 × Height (cm) − 42.8, when actual weight > predicted, the predicted weight should be used in the equations.
dSex, male = 1, female = 2; age, years; height, centimeters.

Statistical analysis

Data are presented as mean ± SD for continuous variables and numbers (%) for categorical variables. Cardiopulmonary responses at maximal exercise between genders were analyzed by student’s t-test. We compared actual VO2 max with predicted VO2 max using repeated-measures ANOVA test with Bonferroni post hoc test. Bland-Altman test was applied to assess agreement between actual measured VO2 max and predicted VO2 max for each prediction equations. All tests were two-sided, and P value < 0.05 was considered statistically significant. We performed all analyses using SPSS software (version 24.0; SPSS, Chicago, IL, USA).

Ethics statement

The study protocol was approved by the Institutional Review Board (IRB) of the Asan Medical Center (IRB No. 2021-0915), which waived the requirement of informed consent because of the retrospective nature of the analysis.

RESULTS

Clinical characteristics of study subject

In this study, 50 patients (mean age, 65 ± 13 years, 74% [37/50] males) fulfilled the enrolled criteria. Smoking history was noted: non-smokers, 19 (38%); current-smokers, 12 (24%); and ex-smokers, 19 (38%). The study group comprised of subjects with lung cancer (n = 29, 58%) and healthy person (n = 21, 42%). Of them, 4% were underweight (body mass index [BMI] < 18.5 kg/m2) and 28% were overweight (BMI > 25 kg/m2). The subjects resting respiratory function results were normal. Table 2 shows the gender-based characteristics of the study subjects.
Table 2

Baseline characteristics of patients

jkms-37-e113-i002
Variables Male (n = 37) Female (n = 13) Total (N = 50)
Age, yr 67 ± 13 60 ± 14 65 ± 13
Height, cm 165 ± 7 157 ± 5 163 ± 7.4
Weight, kg 64.8 ± 12.4 60.2 ± 10.9 64 ± 12.1
Ideal weight, kg 70 ± 5.5 59.4 ± 3.2 67 ± 6.8
BMI, kg/m2 23.7 ± 3.7 24.3 ± 3.8 23.9 ± 3.7
FVC, L 3.6 ± 0.6 3 ± 0.5 3.5 ± 0.6
FVC % predicted 86.2 ± 9.8 94.4 ± 13.3 88.3 ± 11.2
FEV1, L 2.7 ± 0.5 2.3 ± 0.4 2.6 ± 0.5
FEV1 % predicted 92.2 ± 7.9 98.5 ± 11.6 93.8 ± 9.3
FEV1/FVC, % 77.3 ± 7.2 81.4 ± 5.3 78.4 ± 7
VC, L 3.5 ± 0.8 2.5 ± 0 3.4 ± 0.8
MVV, L/min 118 ± 77 96 ± 20 112 ± 68
Activity level, %
Low 56.8 61.5 58
Moderate 40.5 30.8 38
High 2.7 7.7 4
Values are expressed as the mean ± SD and activity level are graded by international physical activity questionnaire, which is expressed as percentage.
BMI = body mass index, FVC = forced vital capacity, FEV1 = forced expiratory volume in one second, VC = vital capacity, MVV = maximal voluntary ventilation.

Variables at maximal exercise

CPET results were as follows: absolute VO2 max, 1.2 ± 0.3 L/min; body weight referenced VO2 max, 20 ± 3.9 mL/kg/min; peak work rate, 94 ± 24 watts; peak heart rate, 142 ± 21 bpm; peak O2 pulse, 10 ± 3 mL/beat; minute ventilation, 59 ± 14 L/min; peak respiratory rate, 34 ± 6 breaths per minute; and peak breathing reserve, 41 ± 18%. VO2 max, peak work rate and peak O2 pulse were higher in male than in female, but not statistically significant (Table 3). Minute ventilation was significantly higher in male than in female. There were no statistically significant difference in VO2 max, peak heart rate, peak O2 pulse, minute ventilation and peak breathing reserve except for peak work rate and peak respiratory rate between lung cancer patients and healthy subjects (Table 4).
Table 3

Cardiopulmonary responses at maximal exercise on cycle ergometry in subjects

jkms-37-e113-i003
Variables Male (n = 37) Female (n = 13) P value
VO2 max, L/min 1.3 ± 0.4 1.1 ± 0.3 0.109
VO2 max, mL/kg/min 20 ± 3.9 18 ± 3.7 0.195
Peak WR, watts 97 ± 25 86 ± 21 0.126
Peak HR, bpm 140 ± 20 146 ± 21 0.385
% predicted maximal HR 87 ± 11 88 ± 13 0.739
Peak O2 pulse (mL/beat) 10 ± 4 8 ± 3 0.090
VE 61 ± 16 53 ± 8.4 0.031
Peak RR 34 ± 6 34 ± 6 0.879
Peak BR, % 39 ± 19 45 ± 13 0.294
Values are expressed as the mean ± SD or number (%).
WR = work rate, HR = heart rate, VE = minute ventilation, RR = respiratory rate, BR = breathing reserve.
Table 4

Cardiopulmonary responses at maximal exercise on cycle ergometry between lung cancer patients and healthy subjects

jkms-37-e113-i004
Variables Lung cancer (n = 29) Healthy subject (n = 21) P value
VO2 max, L/min 1.2 ± 0.3 1.1 ± 0.3 0.148
VO2 max, mL/kg/min 19 ± 3.7 18 ± 3.7 0.612
Peak WR, watts 88 ± 19 86 ± 21 0.032
Peak HR, bpm 139 ± 22 146 ± 21 0.372
Peak O2 pulse, mL/beat 9 ± 2 8 ± 3 0.227
VE 58 ± 14 53 ± 8.4 0.519
Peak RR 32 ± 6 34 ± 6 0.009
Peak BR, % 41 ± 17 45 ± 13 0.973
Values are expressed as the mean ± SD or number (%).
WR = work rate, HR = heart rate, VE = minute ventilation, RR = respiratory rate, BR = breathing reserve.

Comparison between actual absolute VO2 max and predicted absolute VO2 max

Fig. 2 illustrates the marked difference between actual and predicted absolute VO2 max (P < 0.001). Except for predicted absolute VO2 max using Yaoshan prediction equation developed using the Chinese equation, predicted absolute VO2 max were significantly overestimated compared with actual measured absolute VO2 max. Agreement using Bland-Altman test between actual absolute VO2 max and predicted absolute VO2 max was the best in Yaoshan equation (−0.03, 2SD = 0.55) compared to Jones (0.42, 2SD = 1.07), Hansen (0.44, 2SD = 0.86) and Wasserman (0.42, 2SD = 0.86) equations.
Fig. 2

Comparison of actual and predicted absolute VO2 max among subjects. Figure shows significant overestimation of predicted VO2 max compared with actual VO2 max in our population except for predicted VO2 max using Yaoshan equation.

*P < 0.001 for analysis of variance with Bonferroni post hoc pairwise analysis.
jkms-37-e113-g002

DISCUSSION

To the best of our knowledge, this is the first study to select fitted prediction equations for VO2 max by comparing actual absolute VO2 max and predicted absolute VO2 max in Korean adults. We showed that predicted absolute VO2 max using Yaoshan equation was similar to actual absolute VO2 max. Furthermore, most prediction equations for VO2 max developed by primarily Caucasian population overestimated VO2 max in our population.
The value of VO2 max is affected by many factors such as age, sex, height, weight, and physical activity. Thus, the ATS/ACCP for CPET recommends selecting proper reference value that reflects characteristics of their population tested.8 In our study, among various prediction equations, the Yaoshan equation developed using a Chinese population was the most suitable. Because the anthropometric features of Chinese population is similar to those of the Korean population, Yaoshan equation might be appropriate for VO2 max in our study. According to recommendations by ATS/ACCP for CPET, prediction equation by Jones et al.10 and Hansen et al.,11 which were two most generally used equations of reference values, should be applied clinically. However, in our study, predicted absolute VO2 max by Jones et al.10 and Hansen et al.11 was overestimated compared to the actual absolute VO2 max. As in our study, Ahmadian et al.18 showed significant overestimation of predicted VO2 max compared with actual VO2 max using prediction equations by Jones et al.10 and Hansen et al.11 It is necessary to select appropriate sets of reference values for each institution.
Because the most of prediction equation are based on weight and height, VO2 max is greatly affected by anthropometric characteristics. Anthropometric features such as weight and height of the Caucasian and Asian population are different. For example, height, weight and BMI of subjects in an Asian population14161920212223 were similar to those of the present study, but lower than those of primarily Caucasians.121318 As above, the predicted VO2 max using Yaoshan equation using the Asian population had good agreement with our study. The most plausible explanation for good agreement is that the anthropometric characteristics are similar. Therefore, when selecting reference value, it is important to select a reference value that reflects the characteristics of each population well.
In the present study, actual VO2 max was lower than that of other studies by Caucasian population.131824 This is consistent with a previous study that reported that VO2 max in an Asian-Indian population was lower than in a Caucasian population.25 It is crucial to apply reference values specific to different population as VO2 max are affected by ethnic groups. In addition to difference of height and weight, physiology of skeletal muscle, parenchymal lung and chest wall anatomy could have affected to exercise capacity from other ethnicities. In some study with Asian population, lung volumes such as total lung capacity and functional residual capacity are lower than those for Caucasian population.2627
The limitations of this study must be considered. First, this was a retrospective study conducted in a single tertiary referral center in Korea. Because the anthropometric characteristics of subjects may differ depending on the regions of residence, our results cannot be readily applied to the general population in Korea. Second, the possibility of selection bias should be considered because the study population included healthy subjects and early lung cancer patients. The study population may be less healthy than the general population. But early lung cancer patients had normal lung function and normal cardiopulmonary function. Third, most of the enrolled patients were elderly. Fourth, the sex ratio in this study was not 1:1 and the number of included subjects was small. The results of our study may not be generalized to the general population because the number of patients was small, study population is mainly older people, and gender ratio is not 1:1. Further multicenter studies with larger numbers of subject and subjects with all age ranges are warranted to validate our results.
In conclusion, most prediction equations for VO2 max based on Caucasian population yield overestimated VO2 max compared with actual VO2 max. The predicted VO2 max using equation developed using the Chinese population was similar to actual VO2 max. These results imply that the reference value and prediction equation from studies in which populations were primarily Caucasians may not be appropriate for Koreans. Since the mean difference is the lowest in Chinese equation, the Chinese equation might be used for the Korean adult population.

Notes

Disclosure: The authors have no potential conflicts of interest to disclose.

Author Contributions:

  • Conceptualization: Lee JS, Jeong DH.

  • Data curation: Oh YM, Lee SW, Lee SD.

  • Formal analysis: Jeong DH.

  • Investigation: Oh YM, Lee SW, Lee SD.

  • Methodology: Lee JS, Jeong DH.

  • Writing - original draft: Jeong DH.

  • Writing - review & editing: Lee JS.

References

1. Laveneziana P, Di Paolo M, Palange P. The clinical value of cardiopulmonary exercise testing in the modern era. Eur Respir Rev. 2021; 30(159):200187. PMID: 33408087.
crossref
2. Myers J, Prakash M, Froelicher V, Do D, Partington S, Atwood JE. Exercise capacity and mortality among men referred for exercise testing. N Engl J Med. 2002; 346(11):793–801. PMID: 11893790.
crossref
3. Palange P, Ward SA, Carlsen KH, Casaburi R, Gallagher CG, Gosselink R, et al. Recommendations on the use of exercise testing in clinical practice. Eur Respir J. 2007; 29(1):185–209. PMID: 17197484.
crossref
4. Kim HJ, Park SW, Cho BR, Hong SH, Park PW, Hong KP. The role of cardiopulmonary exercise test in mitral and aortic regurgitation: it can predict post-operative results. Korean J Intern Med. 2003; 18(1):35–39. PMID: 12760266.
crossref
5. Hwang TW, Kim SO, Kim MS, Jang SI, Kim SH, Lee SY, et al. Short-term change of exercise capacity in patients with pulmonary valve replacement after tetralogy of fallot repair. Korean Circ J. 2017; 47(2):254–262. PMID: 28382082.
crossref
6. Kim GB, Kwon BS, Choi EY, Bae EJ, Noh CI, Yun YS, et al. Usefulness of the cardiopulmonary exercise test in congenital heart disease. Korean Circ J. 2007; 37(10):489–496.
crossref
7. Kim JY, Yun BS, Lee S, Jung SY, Choi JY, Kim NK. Changes in strain pattern and exercise capacity after transcatheter closure of atrial septal defects. Korean Circ J. 2017; 47(2):245–253. PMID: 28382081.
crossref
8. American Thoracic Society. American College of Chest Physicians. ATS/ACCP Statement on cardiopulmonary exercise testing. Am J Respir Crit Care Med. 2003; 167(2):211–277. PMID: 12524257.
9. Paap D, Takken T. Reference values for cardiopulmonary exercise testing in healthy adults: a systematic review. Expert Rev Cardiovasc Ther. 2014; 12(12):1439–1453. PMID: 25418758.
crossref
10. Jones NL, Makrides L, Hitchcock C, Chypchar T, McCartney N. Normal standards for an incremental progressive cycle ergometer test. Am Rev Respir Dis. 1985; 131(5):700–708. PMID: 3923878.
11. Hansen JE, Sue DY, Wasserman K. Predicted values for clinical exercise testing. Am Rev Respir Dis. 1984; 129(2 Pt 2):S49–S55. PMID: 6421218.
12. Wasserman K. Principles of Exercise Testing and Interpretation: Including Pathophysiology and Clinical Applications. 5th ed. Philadelphia, PA, USA: Wolters Kluwer Health/Lippincott Williams & Wilkins;2012. p. 572.
13. Koch B, Schäper C, Ittermann T, Spielhagen T, Dörr M, Völzke H, et al. Reference values for cardiopulmonary exercise testing in healthy volunteers: the SHIP study. Eur Respir J. 2009; 33(2):389–397. PMID: 18768575.
crossref
14. Dun Y, Olson TP, Li C, Qiu L, Fu S, Cao Z, et al. Characteristics and reference values for cardiopulmonary exercise testing in the adult Chinese population - The Xiangya hospital exercise testing project (the X-ET project). Int J Cardiol. 2021; 332:15–21. PMID: 33716041.
crossref
15. Mohammad MM, Dadashpour S, Adimi P. Predicted values of cardiopulmonary exercise testing in healthy individuals (a pilot study). Tanaffos. 2012; 11(1):18–25.
16. Ong KC, Loo CM, Ong YY, Chan SP, Earnest A, Saw SM. Predictive values for cardiopulmonary exercise testing in sedentary Chinese adults. Respirology. 2002; 7(3):225–231. PMID: 12153688.
crossref
17. Craig CL, Marshall AL, Sjöström M, Bauman AE, Booth ML, Ainsworth BE, et al. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 2003; 35(8):1381–1395. PMID: 12900694.
crossref
18. Ahmadian HR, Sclafani JJ, Emmons EE, Morris MJ, Leclerc KM, Slim AM. Comparison of predicted exercise capacity equations and the effect of actual versus ideal body weight among subjects undergoing cardiopulmonary exercise testing. Cardiol Res Pract. 2013; 2013:940170. PMID: 23653881.
crossref
19. Itoh H, Ajisaka R, Koike A, Makita S, Omiya K, Kato Y, et al. Heart rate and blood pressure response to ramp exercise and exercise capacity in relation to age, gender, and mode of exercise in a healthy population. J Cardiol. 2013; 61(1):71–78. PMID: 23182944.
crossref
20. Yu R, Yau F, Ho S, Woo J. Cardiorespiratory fitness and its association with body composition and physical activity in Hong Kong Chinese women aged from 55 to 94 years. Maturitas. 2011; 69(4):348–353. PMID: 21683535.
crossref
21. Jee Y, Kim Y, Jee SH, Ryu M. Exercise and cancer mortality in Korean men and women: a prospective cohort study. BMC Public Health. 2018; 18(1):761. PMID: 29914427.
crossref
22. Kim BJ, Kim Y, Oh J, Jang J, Kang SM. Characteristics and safety of cardiopulmonary exercise testing in elderly patients with cardiovascular diseases in Korea. Yonsei Med J. 2019; 60(6):547–553. PMID: 31124338.
crossref
23. Kim YH, Shim WJ, Kim MA, Hong KS, Shin MS, Park SM, et al. Utility of pretest probability and exercise treadmill test in Korean women with suspected coronary artery disease. J Womens Health (Larchmt). 2016; 25(6):617–622. PMID: 26562494.
crossref
24. Kaminsky LA, Arena R, Myers J. Reference standards for cardiorespiratory fitness measured with cardiopulmonary exercise testing: data from the fitness registry and the importance of exercise national database. Mayo Clin Proc. 2015; 90(11):1515–1523. PMID: 26455884.
crossref
25. John N, Thangakunam B, Devasahayam AJ, Peravali V, Christopher DJ. Maximal oxygen uptake is lower for a healthy Indian population compared to white populations. J Cardiopulm Rehabil Prev. 2011; 31(5):322–327. PMID: 21734591.
crossref
26. Singh R, Singh HJ, Sirisinghe RG. Spirometric studies in Malaysians between 13 and 69 years of age. Med J Malaysia. 1993; 48(2):175–184. PMID: 8350793.
27. Vijayan VK, Kuppurao KV, Venkatesan P, Sankaran K, Prabhakar R. Pulmonary function in healthy young adult Indians in Madras. Thorax. 1990; 45(8):611–615. PMID: 2402724.
crossref
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