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�:	Use of The Oxygen Uptake Efficiency Slope to Measure Cardiorespiratory Function in Intellectual Disabilities

Tamotsu Yabumoto1*, Reizo Baba2,Tsuneo Watanabe1, Sohee Shin1, Bateer Shi1, Naoki Sakakibara1, Osamu Fukutomi3,Toshio Matsuoka1
1 Gifu University Graduate School of Medicine
2 Aichi children�s Health and Medical center
3 Fukutomi children�s clinic

Author Note
We have no conflicts of interest in the sponsorship of our study. 
Tamotsu Yabumoto, Tsuneo Watanabe, Sohee Shin, Bateer Shi, Naoki Sakakibara, and Toshio Matsuoka are with the Department of Sports Medicine and Sports Science, Gifu University Graduate School of Medicine, 1-1 yanagido, Gifu, Gifu 501-1194 Japan. Reizo Baba is with the Aichi children�s Health and Medical center, 1-2 osakada, morioka, oubu, Aichi 474-871 Japan. Osamu Fukutomi is with Fukutomi children�s clinic, 1228 ajiki, Gifu, Gifu 501-1109 Japan.

Correspondence to:0Tamotsu Yabumoto, Department of Sports Medicine and Sports Science,  Gifu University Graduate School of Medicine, 1-1, Yanagido, Gifu, 501-1194, Japan, Tel: +81-58-230-6424; Fax: +81-58-230-6425; E-mail : o2111604@edu.gifu-u.ac.jp
Background: The purpose of this study was to determine the efficacy and suitability of the oxygen intake efficiency incline (Oxygen Uptake Efficiency Slope; OUES) to assess cardiorespiratory fitness in intellectually disabled (ID) individuals. Methods: We studied 48 sedentary ID individuals using a bicycle ergometer. Analysis of exhaled gas was performed using an exhalation gas-measuring assembly, and estimating the oxygen intake (VO2: ml/min) and ventilatory volume (VE: l/min) by the breath-by-breath method. As an index of the exercise performance, peak VO2, ventilation threshold (VT), and OUES were measured. OUES was calculated at the time of 3 reaching movements of 60% HR max (OUES60), 80% HR max (OUES80), and peak HR (OUES100) by relative exercise intensity (% HR max) using the predictive maximal heart rate (220-age). Results: Of the 48 participants, 13 (27.1%) did not reach a peak respiratory exchange ratio (RER) of 1.09, and 35 subjects (72.9%) exceeded this value. A highly significant correlation was observed between OUES and peak VO2 (r = 0.88 P < 0.01), whereas a moderately significant correlation was found between VT and peak VO2 (r = 0.68 P < 0.01). No significant differences were found between OUES100, OUES60, and OUES80 in the maximal effort group. Conclusion: OUES of ID individuals are related to peak VO2, are not influenced by exercise intensity, and can be used to evaluate cardiorespiratory evaluation at approximately 60% submaximal exercise load intensity of the predictive maximal heart rate.
Keywords: oxygen uptake efficiency slope, intellectual disabilities, cardiorespiratory, evaluation

Introduction
Maximum oxygen intake (VO2 max) is commonly used in exercise testing to assess an individual�s endurance capacity. Maximal effort is required to measure the VO2 max. Therefore, we assumed that individuals with an intellectual disability (ID) may not be able to reach VO2 max as it can be difficult to provide clear instructions and incentives to this group. Although the endurance capacity of an ID is reportedly lower than that of healthy subjects, the motivation to attain maximal effort may have influenced the results [6-9, 14,15,19]. Furthermore, an ID may not assess fatigue precisely, and assessment of exercise capacity using methods requiring peak load may be dangerous in this group. Given these potential complications, an evaluation index that does not require a maximal effort is necessary to properly and reliably assess exercise endurance in an ID.
Recently, the oxygen intake efficiency incline (Oxygen Uptake Efficiency Slope: OUES) has been proposed as a new index of endurance measurement, which does not require a subject to reach full fatigue [1-3]. The OUES is derived from the logarithmic relation between oxygen consumption (VO2) and minute ventilation (VE) during incremental exercise. The OUES is an objective, reproducible measure of cardiopulmonary reserve that does not require a maximal exercise effort [11]. Several reports suggest that this approach is suitable for patients who are at high risk of a cardiovascular event by maximal exercise, because of disorders such as lung cancer or heart disease [4,5,16].
The purpose of this study was to determine the efficacy and suitability of the OUES to assess cardiorespiratory fitness in ID. 

Material and Methods
Participants
We studied 40 sedentary ID, who were of high-school age and enrolled at a school for children with special needs. This study was approved by the institutional ethics committee, and written informed consent was obtained from all participants. In our cohort, the degree of the intellectual impairment was deemed to be mild (IQ, 50�70). Exclusion criteria for this study included a history of heart disorders and extreme obesity (BMI > 25) (Table1). 

Experimental Set-up
Prior to beginning the experiment, a practice session of approximately 1 h was conducted to allow proper adjustment of the test mask and pedals. The exercise test device used was a bicycle ergometer (Well Bike BE-360, Fukuda Denshi, Tokyo, Japan). The exercise test protocol followed the ramp load method, with 5 min rest periods. The ramp load was started at 30 W after a warm-up period with no load for 3 min. The ramp load was increased by 15 W each minute. We terminated the exercise whenever the participant was no longer able to maintain a pedaling rate of 60 rpm. We measured VO2 and peak VO2 at this time-point. The pedaling speed may be affected by the degree of intellectual impairment of the subjects. Participants were encouraged to maintain a fixed pace by a teacher and a bleeping noise from the speedometer. Analysis of exhaled gas was performed using an exhalation gas-measuring assembly (Oxycon Alpha, Mijnhard, The Netherlands). Oxygen intake (VO2: ml/min) and ventilatory volume (VE: l/min) were measured using the breath-by-breath method. 

Analysis of VO2 max
The evaluation was conducted at exhaustion and 2 points of view of the exercise performance were considered. We used the optimal heart rate (peak HR) as an index for reaching intensity, and also used the optimal respiratory exchange ratio (peak RER) because of the likelihood that a heartbeat reply was not performed appropriately in ID. We examined the association between each index of exercise performance. An RER exceeding 1.09 was taken as requiring a maximal effort [10].
As an index of exercise performance, peak VO2, ventilation threshold�VT), and the OUES were assessed. Peak VO2 had an exercise terminal mean of 30 s. VT was calculated by V-slope. The OUES was calculated using a similar logarithmic function of minute ventilation (VE) with VO2 in an exercise test. We performed a coefficient of item log of this time with OUES (Figure 1). OUES was calculated at the time of 3 reaching movements of 60% HR max (OUES60), 80% HR max (OUES80), and peak HR (OUES100) by relative exercise intensity (% HR max) using the predictive maximal heart rate (220-age). We correlated VT, peak VO2, and the OUES at the time of each reaching movement. Furthermore, we examined the OUES and the difference in every % HR max in peak VO2 to determine the influence of reaching movement intensity on the index. Moreover, Bland-Altman analysis was performed between OUES100 and OUES80, as well as OUES100 and OUES60 to determine the presence or absence of a systematic error in the results. 

Statistical Analysis
Data were analyzed using SPSS software (version 13.0J, SPSS Inc, Chicago, IL, USA). Pearson�s correlation coefficients were used to investigate the correlation between 2 values. Significant differences between groups were assessed by single regression analysis of variance. Results are presented as mean � standard deviation (SD) and statistical significance was set at p < .05. 

Results
Reaching exercise intensity of ID 
Of the 40 participants, 12 (30.0%) did not reach a peak RER of 1.09, and 28 subjects (70.0%) exceeded this value. Any participant with an RER value of greater than 1.1 was placed in the �maximal effort group�. However, none of the subjects within this group reached the predictive maximal heart rate (220-age).

Relationship between the OUES and other cardiorespiratory function measures
     OUES values were well correlated with peak VO2 (r = 0.89 p < .01), while the correlation between VO2 and VT was highly significant (r = 0.64 p < .01). A good correlation was also found between the values of VT and OUES (r = 0.42 p < .01) (Figure. 2).

Relations between OUES and load intensity
No significant difference was found between OUES100, OUES80, and OUES60 in the maximal effort group. However, peak VO2 was higher in the VO2100 compared with the VO280 (p < .05) and VO260 (p < .01) in the maximal effort group (Figure. 3).
Bland-Altman analyses indicated no addition or proportion errors in OUES100 and OUES80, both of OUES60. The tolerance level (Limit of agreement (LOA) of the error between measurements) was -305.9 � 271.0 in OUES100 and OUES80, and was -525.6 � 523.5 in OUES100 and OUES60, respectively (Figure. 4).

Discussion
The findings of this study show that the OUES is useful to determine submaximal endurance in ID and may potentially serve as a method for the measurement of the actual peak VO2. The finding that almost a quarter of ID in the present investigation did not achieve peak VO2 underlines the need for an alternative measurement of submaximal fitness in such individuals. Our results suggest that the OUES is reliable and a more useful measurement of submaximal fitness than the VT. Assessing cardiorespiratory fitness in people with ID is difficult because of variations in the testing methodologies and performance of the participants due to learning or motivational impairments [13,17,20,21]. Therefore, it is unclear whether the observed poor score results from poor cardiorespiratory fitness or the inability of subjects to perform optimally on the test. 
In this study, 30.0% of cases displayed an RER <1.09. Lack of motivation among study participants may have influenced these results. Moreover, the one subject who did exceed an RER value of 1.09 did not reach the predicted maximal heart rate. This was attributed to difficulty in reaching maximal endurance by the ID, and suggests that an appropriate heartbeat reply was not obtained even if a maximal effort was made. Therefore, we employed a submaximal index when we performed exercise testing in ID. We believed it was important for risk management to be scattered with a varied clinical index, with the exception of any of the exclusion criteria. 
The OUES of the maximal effort group whose RER exceeded 1.09 was related to the evaluation index for endurance. OUES was significantly and positively correlated with VO2 max, suggesting that the OUES may be a valid means of testing endurance in this cohort. Furthermore, the coefficient of correlation between OUES and peak VO2 was higher than that between peak VO2 and VT. VT is a commonly used index to evaluate endurance under a maximum effort. However, many of the parameters used in calculating VT are quite subjective. In addition to the OUES being highly correlated with peak VO2, this index may be more suitable to evaluate whole body stamina evaluation than VT since the measurement parameters are less subjective.
There were no significant differences in the load intensities of OUES100, OUES80, and a value of OUES60 that we set based on a predictive maximal heart rate. However, peak VO2 tended to be on the lower end of the scale when load intensity was also low. Results were thought to be equivalent to a maximal effort if reaching movement intensity was 60% of predictive maximal heart rate. Load intensity was found to affect OUES because the range of error decreased to facilitate an increase in the reaching intensity. We assumed that this was equivalent to maximal effort in patients with heart disorders, elderly people, and obese subjects during maximal intensity. This was also equivalent to approximately 60% of the residual heartbeat function at reaching movement time [10,12,18]. In addition, our data indicate that OUES80 and OUES60 provide a non-biased and reliable measure of OUES100 (Figure 3) in ID. These observations suggest that a reliable measure of OUES can be obtained using incremental exercises of relatively short duration and of submaximal intensity, provided that the subject reaches at least OUES60. Increasing the exercise duration up to OUES80 will further increase the confidence of OUES determination. 
Conclusion
 OUES of ID are related to peak VO2, are not influenced by exercise intensity, and can be used to evaluate cardiorespiratory evaluation at approximately 60% submaximal exercise load intensity of the predictive maximal heart rate.
References
1.  Baba R, Nagashima M, Goto M, Nagano Y, Yokota M, et al. (1996) Oxygen uptake efficiency slope: a new index of cardiorespiratory functional reserve derived from the relation between oxygen uptake and minute ventilation during incremental exercise. Journal of the American Colledge of Cardiology 28: 1567-1572. 
2.  Baba R, Nagashima M, Nagano Y, Ikoma M, Nishibata K (1999) Role of the oxygen uptake efficiency slope in evaluating exercise tolerance. Archives of Disease in Childhood 81: 73-75. 
3.  Baba R, Tsuyuki K, Kimura Y, Ninomiya K, Aihara M, et al. (1999) Oxygen uptake efficiency slope as a useful measure of cardiorespiratory functional reserve in adult cardiac patients. European Journal of Apliedl Physiology and Occupational Physiology 80: 397-401. 
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DISCLOSURES
 No conflicts of interest

Table 1 Mean and standard deviation (SD) values of relevant physiological variables of the subjects included in the study	
Variable		 Males0     SD	0  Females	   SD
		       (n = 26)	           (n = 14)	
Age (years)	        16.0	0     0.8	0 0 16.0000  00.9
Body weight (kg)      61.9	      14.8	0    54.4*	     11.5
Height (cm)	       166.3	 0    8.0	0   153.7*000 07.9
BMI (kg/m2)           22.2	 0    4.5	0    23.00	      4.6
*indicates a significant difference (p < .05) compared with males			
FIGURE LEGEND
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Figure 2: Individual values of OUES100 and peak VO2 (left), VT and peak VO2 (center), and OUES100 and VT (right). Regression lines, equations, and correlation coefficients are shown.

Figure  3: OUES values calculated from the data obtained from 60% (OUES60), 80% (OUES80), and peak HR (OUES100) of the predictive HR max (left), and VO2 values calculated from the data obtained from 60% (VO260), 80% (VO280), and peak HR (VO2100) of the predictive HR max (right). Values are presented as the mean (SD).* p < .05, ** p < .01

Figure 4: Bland-Altman plots indicating the mean difference (bias) between measures of OUES80 and OUES100 (left), and OUES60 and OUES100 (right), as a function of the mean of the 2 measures. Values of the SD (precision) and the 95% limits of agreement are also reported for each graph. 










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