Pulmonary Function in Obese Subjects
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1 ulmonary Function in Obese Subjects a Normal FEV^FVC Ratio* Hamid Sahebjami, MD, FCC; and eter S. Gartside, hd Study objective: To determine pulmonary function test (FT) profile and respiratory muscle strength (RMS) of a group of obese individuals who did not have evidence of obstructive airway disease or other underlying diseases affecting their respiratory system. Design: rospective, open. Setting: FT laboratory, VA Medical Center. articipants: Sixty-three consecutive obese (body mass index greater than 27.8 kg/m2) male subjects without overt obstructive airway disease (FEVi/FVC ratio greater than 80%). Measurements and results: Standard FTs and maximum static inspiratory (imax) and expiratory (Emax) mouth pressures were determined. RMS was calculated from the following formula: (Imax+Emax):2. Two distinct groups were identified, those with normal maximum voluntary ventilation (MW) (>80% predicted) and those with low MW. Both inspiratory and expiratory flow rates (FVC, FEVi, forced expiratory flow at 50% vital capacity [V50L maximum inspiratory flow rate [MIFR]), lung volumes (vital capacity [VC], inspiratory capacity [IC], expiratory reserve volume), imax, and RMS were significantly lower, and residual volume/total lung capacity (RV/TLC) ratio was significantly higher in obese subjects with low MW compared with those in whom MW was normal. MW correlated significantly with FVC, FEV,, V50, MIFR, TLC, VC, IC, RV/TLC, and RMS; the strongest correlation was with MIFR (r=0.76, p<). Conclusions: Standard FTs allow recognition of a subgroup of obese subjects without overt obstructive airway disease who have more severe lung dysfunction, the marker ofwhich is a low MW. eripheral airway abnormalities may be responsible for these observations. (CHEST 1996; 110: ) Key words: inspiratory flow rates; maximum voluntary ventilation; pulmonary function tests; respiratory muscles; small airways Abbreviations: ABG=arterial blood gas; BMI=body mass index; Deo=diffusing capacity for carbon monoxide; ERV=expiratory reserve volume; FRC=functional residual capacity; IC=inspiratory capacity; MIFR=maximum inspiratory flow rate; MW=maximum voluntary ventilation; Emax=maximum static expiratory mouth pressure; FT=pufmonary function test; Imax=maximum static inspiratory mouth pressure; RMS=respiratory muscle strength; RV=residual volume; TLC=total lung capacity; VC=vital capacity; V,5o=forced expiratory flow at 50% VC Tt is well known that obesity alone, in the absence of -*. other disease processes, affects respiratory function in humans. The most persistent pulmonary function test (FT) abnormalities in obesity are reduced expi ratory reserve volume (ERV) and functional residual capacity (FRC) due to alterations in chest wall me chanics,1" ' which also leads to decreased total respira tory compliance.2' Obese, nonsmoking individuals may also have reduced vital capacity (VC), total lung capacity (TLC), and forced expiratory flow rates at low lung volumes associated with increased residual vol- *From the ulmonary Section, Department of Veterans Affairs Medical Center, and University ofcincinnati (Ohio) College of Medicine. Manuscript received April 11, 1996; revision accepted June 10. Reprint requests: Dr. Sahebjami, ulmonary Section (11 IF), VA Medical Center, 3200 Vine Street, Cincinnati, OH ume (RV), RV/TLC ratio, and airway resistance; the latter three findings are suggestive ofperipheral airway disease.89 Total respiratory resistance and work are also increased in obesity.10 Maximum voluntary ventilation (MW) can be low1'2'4'5'11 or normal9'12'13 in obese indi viduals. These FT abnormalities are more pronounced in massively obese individuals and in those with obesityhypoventilation syndrome. To our knowledge, effects of obesity on inspiratory flows have not been addressed. We studied the FT profile and respiratory muscle strength of a large group of obese individuals who did not have any evidence of significant obstructive airway abnormality or other underlying disease processes af fecting their respiratory system. We describe two dis tinct groups of obese subjects based on their FT profiles and discuss the potential pathophysiologic state responsible for the differences. CHEST /110 / 6 / DECEMBER,
2 Table 1.Characteristics of Obese Subjects* Age, yr Mean 43.9 Range BMI, kg/m2 Mean 36.7 Range Smoking history, No. (%) Current 5 (23.8) revious 2 (9.5) Never 14 (66.7) Hypercapnia,1 No. (%) 1 (5.2) (aco2 >45 mm Hg) Hypoxemia,1 No. (%) 9 (47.3) (ao2 <80 mm Hg) (38.1) 10 (23.8) 16 (38.1) 9 (25.0) 28 (77.7) * Numbers inside parentheses indicate percent of total in each group. *ABG data were available in 19 subjects with normal MW and in 37 subjects with low MW. Materials and Methods Study opulation During a 12-month period, all subjects referred to the ulmonary Function Laboratory at the Cincinnati Veterans Affairs Medical Center were screened for the presence of obesity in the absence of obstructive airway disease. The obesity was defined to exist when body mass index (BMI) was greater than 27.8 kg/m2,14,15 and the absence of obstructive airway disease was determined by a FEVi/ FVC ratio of greater than 80%. Subjects' chnical records, chest ra diographs, and other relevant data were reviewed to identify and eliminate those with underlying diseases that could have affected their pulmonary function. The study was approved by our Institu tional Review Board. Measurements Body weight and height were measured with subjects wearing indoor clothing and shoes with 2.5-cm heels, and BMI was calcu lated as body Flow weight/height2. rates, lung volumes, and single-breath carbon monoxide diffusing capacity (Deo) were determined using automated equip ment (Collins model GS/lus; Warren E. Collins Inc; Braintree, Mass). Forced inspiratory and expiratory maneuvers were per formed three times and the best values obtained from the maximum inspiratory and expiratory flow-volume curves were used for com parison. FRC was measured by the nitrogen washout technique, and RV was obtained as FRC minus ERV. TLC was calculated as RV plus VC. Single-breath Deo was performed in duplicate and the larger value was reported. Recommendations for standardized procedures for various lung function test measurements were followed.16"18 MW was determined after instructing the subject to breathe as fast and as deep as he could for a period of 12 s. If the frequency of breathing was less than 60 min-1 and the tidal volume was less than 40% of VC on the first maneuver, the patient was instructed to breathe faster and deeper on the next maneuver; the greatest of the two efforts was used for comparison.9 Reference predicted values from the following reports were used to assess various FTs: Knudson and associates19 for spirometry, Goldman and Becklake20 for lung volumes, Baldwin and associates21 for MW, and Gaensler and Smith22 for Deo. Maximum static inspiratory (imax) and ex piratory (Emax) mouth pressures were measured at RV and TLC, respectively, using the method of Black and Hyatt.23 An index of respiratory muscle strength (RMS) w7as calculated from (Imax+ Emax) :2 according to Aldrich et al.24 Arterial blood samples were drawn from the radial artery with the patient in a sitting position while breathing room air. Arterial blood gas (ABG) analysis was performed using the ABG-520 (Radiome ter American Inc; Wesdake, Ohio). Statistical Analysis For each parameter measured or calculated, the values for indi vidual patients were averaged per group, and the SEM was calcu lated. Differences between the two groups were tested by an un paired Student's t test; p<0.05 was considered significant. earson product-moment correlation coefficients25 ofvarious FT values on percent MW, as the dependent variable, were compared. Results Sixty-three obese male subjects without significant obstructive airway disease were studied. Initial assess ment of FT results revealed that two distinct groups could be identified: those with MW greater than 80% predicted (normal MW group), and those in whom MW was lower than 80% predicted (low MW group). Subsequent analysis of data allowed clear and distinct separation of FT profiles in the two groups. We, therefore, decided to discuss the results in the context of differences between these two groups. Some ofthe clinical characteristics ofthe two groups are listed in Table 1. A greater number of subjects with normal MW had never smoked, while a larger num ber of patients with low MW were current smokers. Only 1 subject in the former group (5.2%), but 9 in the latter group (25%) had baseline hypercapnia. Resting room-air hypoxemia was present in 9 (47.3%) subjects with normal MW and in 28 (77.7%) subjects with low MW. Spirometric data are shown in Table 2. Both in spiratory and expiratory flow rates (FVC, FEVi, forced expiratory flow at 50% VC [V50], maximum inspiratory flow rate [MIFR]) were significantly lower in the group with low MW compared with the other group. Based on the selection criteria, FEVi/FVC ratio was above 80% in both groups. Lung volume measurements (Table 3) revealed that VC, inspiratory capacity (IC), and ERV were lower Table 2.Spirometric arameters in Obese Subjects* FVC, %pred FEVi, %pred FEVi/FVC, % V50, L/s MIFR, L/s MW, %pred MW, L/min * s are means ± SEM. 78.5± ± ± ± ± ± ± ± ± ± ± ± Clinical Investigations
3 TLC, %pred FRC, %pred RV, %pred VC, %pred IC, %pred ERV, %pred Table 3.Lung Volumes in Obese Subjects* RV/TLC, %pred *s are means ± SEM. 76.3± ± ± ± ± LowMW 70.7± ± ± ± ± ± while RV and RV/TLC ratio were higher in subjects with low MW compared with the normal MW group. In obese patients with normal MW, imax and RMS were significantly greater than in those with low MW; the differences in Emax between the two groups reached only borderline significance (Table 4). Groups did not differ in ABG values or Deo (Table 5). MW, as the dependent variable, correlated signif icantly with certain FT parameters (Table 6); the strongest correlation was with MIFR (r=0.76, p<, R2=0.58), as shown in Figure 1. Addition of FVC, as a second regressor to MIFR, explained 65% of variance in MW (R2=0.65, p=) by multiple regression analysis. Discussion FT abnormalities in Our study revealed significant obese individuals who do not have overt obstructive airway disease. The most distinguishing FT parame ter was MW which allowed further classification ofthe study population into two distinct groups. The FT profile of obese persons with low MW consisted of smaller lung volumes, inspiratory and expiratory flow rates, and RMS but more air trapping. MW was independent of age and BMI but correlated signifi cantly with a variety of FT parameters, the strongest being MIFR (Table 6), which explained 58% of vari ance in MW. We will attempt to discuss the patho of low MW and the usefulness of physiologic standard FTs state in explaining it in some obese subjects. Many factors, including ventilatory mechanics, lung and thoracic cage compliance, RMS, and subjects' motivation and effort affect the MW maneuver Both inspiratory and expiratory flow rates can influ ence the MW measurement.9,24'28"30 Indeed, various Table 4.RMS in Obese Subjects* imax, cm H2O Emax, cm H2O RMS, cm H20 (n=13) 112±9 181+: (n=19) 81±8 145±12 111± Table 5.Gas Exchange arameters in Obese Subjects* a02, mm Hg ac02, mm Hg ph Deo, %pred (n=19) 77.7± ± ± ±4.9 (20) (n=37) 73.6± ± ± ±3.4 (42) *s are means±sem. Numbers in parentheses indicate number of subjects. formulas using FEVi have been suggested to indirectly calculate MW Addition of MIFR and imax to FEVi allows more accurate estimation of MW in normal subjects and in patients with COD.9,26 Fur thermore, MIFR correlates significantly with imax9,30 and both decrease significantly with increased air trapping as represented by elevated RV/TLC ratio.9 The correlation among MIFR, imax, and RV/TLC ratio is most likely the result of air trapping that posi tions the diaphragm at a mechanical disadvantage limiting its ability to generate force and pressure. Al ternatively, diaphragmatic weakness could lead to lower MIFR and imax. Ray and associates31 studied respiratory function in young, nonsmoking obese subjects. Only severely obese individuals had normal results of FTs, includ ing reduced VC, ERV, TLC, FRC, and MW. RV/TLC ratio calculated from mean values was largest in the severely obese subjects. Rubinstien et al8 reported duced FRC, TLC, ERV, FVC, FEVi, and re maximum expiratory flow ratios at low lung volumes and in creased RV, RV/TLC ratio, and airway resistance in markedly obese, nonsmoking men and women. They could not explain mechanism(s) responsible for pe ripheral airway abnormalities in nonsmoking, morbidly obese men. Sharp and associates10 reported increased total res piratory work and decreased respiratory compliance obese normal subjects. Also, in MW was smaller and Table 6.Correlation Between MW (ercent redicted) as the Dependent Variable and Other arameters in All Obese Subjects (n=63) FVC, %pred FEVb % pred V50, L/s MIFR, IVs TLC, %pred VC, %pred IC, %pred RV/TLC, %pred RMS, cm H20 (32)* r * Number in parentheses indicates number of subjects. p CHEST /110 / 6 / DECEMBER,
4 9 8 7 ^ 6 H w * # 1 r = p = MW (% pred) Figure 1. Correlation between MW (percent predicted) and MIFR (L/s) in 63 obese subjects without obstructive airway disease. RV/TLC ratio (calculated from mean values) larger in obese individuals. Naimark and Cherniack2 showed that reduced compliance of the total respiratory system in obese individuals was almost entirely related to reduced chest wall compliance. In 6 of 11 obese subjects, MW was less than 80% predicted. No apparent correlation ex isted between MW and BMI (calculated from indi vidual data). In none of the previous reports of FT results in patients with obesity were inspiratory flow rates mea sured or discussed. Our study population consisted of obese subjects without any known underlying condi tion, which could have had an impact on their lung function, and without overt obstructive airway disease, which could have influenced MW measurements. Compared to subjects with normal MW, a larger per centage of subjects with low MW were current and previous smokers (33.3% vs 61.9% combined) and a smaller percentage were never-smokers (Table 1). Furthermore, a larger percentage of subjects with low MW had hypoxemia and hypercapnia (Table 1). These data alone may suggest that subjects with low MW were, by whatever mechanism(s), more severely af fected as the result of obesity. Indeed, 25% of subjects with low MW, compared with only 5.2% of those with normal MW, were suffering from obesity-hypoventilation, which in previous studies has been associated with more severe respiratory function abnormali ties.1032 Bradley et al32 compared obese patients with obstructive sleep apnea who were hypercapnic during wakefulness with those in whom ac02 was normal. Lung volumes, large and peripheral air flows, and air way resistance were significantly different in the two groups. Again, RV/TLC ratio (calculated from mean values) was markedly larger in the hypercapnic group. In addition to the presence of a larger number of smokers and hypoxemic and hypercapnic subjects among obese patients with low MW in our study, lower inspiratory and expiratory flow rates and RMS and more air trapping were likely responsible for reduced MW. Based on these observations, we be lieve that some obese subjects manifest peripheral airway abnormalities, suggested by reduced maximum expiratory flow rates at low lung volumes and air trap ping. As the result of air trapping, inspiratory muscles are placed at a mechanical disadvantage leading to lower inspiratory pressure and flow, and reduced RMS, causing low MW. Alternatively, in some obese subjects, diaphragmatic muscle weakness due to a va riety of causes could lead to decreased MIFR, imax, and MW. Standard FT parameters allow recognition of a subgroup of obese subjects without overt obstruc tive airway disease who suffer from a more severe pulmonary dysfunction, the marker of which is a low MW. These individuals might benefit from closer observation and more vigorous therapeutic attempts to avoid complications of obesity. References 1 Bedell GN, Wilson WR, Seebohm M. ulmonary function in obese persons. J Clin Invest 1958; 37: Naimark A, Cherniack RM. Compliance ofthe respiratory system and its components in health and obesity. J Appl hysiol 1960; 15: Alexander JK, Amad KH, Cole VW. Observations on some clin ical features of extreme obesity, with particular reference to car diorespiratory effects. Am J Med 1962; 32: Cullen JH, Formel F. The respiratory defects in extreme obe sity. Am J Med 1962; 32: Barrera F, Reidenberg MM, Winters WL. ulmonary function in the obese patient. Am J Med Sci 1967; 254: Luce JM. Respiratory complications of obesity. Chest 1980; 78: Suratt M, Wilhoit SC, Hsiao HS, et al. Compliance ofchest wall in obese subjects. J Appl hysiol 1984; 57: Rubinstein I, Zamel N, DuBarry L, et al. Airflow limitation in morbidly obese, nonsmoking men. Ann Intern Med 1990; 112: Dillard TA, Hnatiuk OW, McCumber TR. Maximum voluntary ventilation: spirometric determinants in chronic obstructive pul monary disease patients and normal subjects. Am Rev Respir Dis 1993; 147: Sharp JT, Henry J, Sweany SK, et al. Effects of mass loading the respiratory system in man. J Appl hysiol 1964; 19: Rochester DF, Enson Y. Current concepts in the pathogenesis of the obesity-hypoventilation syndrome: mechanical and circula tory factors. Am J Med 1974; 57: Gilbert R, Sipple JH, Auchincloss JH. Respiratory control and work of breathing in obese subjects. J Appl hysiol 1961; 16: Kollias J, Boileau RA, Bartlett HL, et al. ulmonary function and physical conditioning in lean and obese subjects. Arch Environ Health 1972; 25: Van Itallie TB. Health implications of overweight and obesity7 the in United States. Ann Intern Med 1985; 103: Sahebjami H, Doers JT, Render ML, et al. Anthropometric and 1428 Clinical Investigations
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