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Original Research: Pulmonary Physiology |

Secular Changes in Relative Leg Length Confound Height-Based Spirometric Reference ValuesSecular Changes in Predicted Lung Function FREE TO VIEW

Philip H. Quanjer, MD, PhD; Masaru Kubota, MD, PhD; Hirosuke Kobayashi, MD, PhD, FCCP; Hisamitsu Omori, MD, PhD; Koichiro Tatsumi, MD, PhD, FCCP; Minoru Kanazawa, MD, PhD; Sanja Stanojevic, PhD; Janet Stocks, PhD; Tim J. Cole, ScD
Author and Funding Information

From the Department of Pulmonary Diseases (Dr Quanjer), and the Department of Paediatrics (Dr Quanjer), Division of Respiratory Medicine, Erasmus University Medical Centre—Sophia Children’s Hospital, Rotterdam, The Netherlands; the Department of Respiratory Medicine, School of Medicine (Dr Kubota), and the Graduate School of Medical Sciences (Dr Kobayashi), Kitasato University, Kanagawa, Japan; the Department of Biomedical Laboratory Sciences (Dr Omori), Faculty of Life Sciences, Kumamoto University, Kuhonji, Chuo-ku, Kumamoto-shi, Kumamoto, Japan; the Department of Respirology (Dr Tatsumi), Graduate School of Medicine, Chiba University, Inohana, Chuo-ku, Chiba-shi, Chiba, Japan; the Department of Respiratory Medicine (Dr Kanazawa), Saitama Medical University, Morohongo, Moroyama, Iruma-gun, Saitama, Japan; the Division of Respiratory Medicine (Dr Stanojevic), The Hospital for Sick Children, Toronto, ON, Canada; Institute of Health Policy, Management, and Evaluation (Dr Stanojevic), University of Toronto, Toronto, ON, Canada; and the Respiratory, Critical Care, and Anaesthesia Section (Portex Unit) (Dr Stocks), and the Population, Policy and Practice Programme (Dr Cole), UCL Institute of Child Health, London, England.

CORRESPONDENCE TO: Philip H. Quanjer, MD, PhD, Department of Pulmonary Diseases and Department of Paediatrics, Division Respiratory Medicine, Erasmus University Medical Centre—Sophia Children’s Hospital, ‘s-Gravendijkwal 230, 3015 CE Rotterdam, The Netherlands; e-mail: pquanjer@gmail.com


FUNDING/SUPPORT: The authors have reported to CHEST that no funding was received for this study.

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details.


Chest. 2015;147(3):792-797. doi:10.1378/chest.14-1365
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BACKGROUND:  Most but not all data from different ethnic groups fit the Global Lung Function Initiative (GLI) spirometric reference model. This study investigates to what extent discrepancies are caused by secular changes in body proportions.

METHODS:  FEV1 and FVC from 20,336 healthy Japanese subjects (13,492 women) aged 17 to 95 years were compared with GLI-2012 reference values for Europeans. Data on the sitting height/standing height ratio (Cormic index) in 17-year-old students, collected from 1949 to 2012 in successive birth cohorts, were used to assess secular changes in body frame. The cohort-specific Cormic index was used to assess how variation in body frame affected pulmonary function.

RESULTS:  FEV1 and FVC were lower than GLI-2012 reference values, with values progressively falling until age 35 to 40 years and then rising to European levels in the elderly. The Cormic index rose until 1942, then fell, with a nadir in the 1970s, before rising again until 1995. Nearly one-half of the spirometric variability from predicted values could be explained by differences in the Cormic index between birth cohorts.

CONCLUSIONS:  In low-income countries, improving health conditions are likely to drive increases in height and changes in relative leg length similar to those observed in Japan and, thus, to a change in body frame. This implies that height-based prediction equations for such populations will need to be periodically updated.

Figures in this Article

Indexes of lung size, such as FEV1 and FVC, and of airways obstruction, such as the lung emptying rate (FEV1/FVC), vary with body dimensions, age, sex, and ethnic group.1 In mammals, lung volumes and flows scale as a power function of body mass.2 However, body mass is not an ideal predictor of pulmonary function in humans, as overweight and underweight are not associated with larger or smaller lungs, respectively. Therefore, standing height is almost universally used as a proxy for lung dimensions and respiratory flows. This is appropriate, provided the relationship between standing height and thoracic dimensions is constant. However, individuals do differ in body frame. Thus, about one-half of the difference in pulmonary function between subjects of African and European origin can be explained by differences in the height of the upper body segment.35 Improved socioeconomic circumstances generally lead to an increase in standing height, driven primarily through increased leg length rather than an increase in upper body height. This gives rise to secular changes in the Cormic index (ie, the sitting height/standing height ratio).68

A number of studies have shown that although reference values from the Global Lung Function Initiative (GLI)1 fit many populations well,9,10 Japanese data do not.11 Over the past 80 years there have been significant changes in body proportions in the Japanese, with leg length increasing faster than sitting height.12,13 The purpose of this study was to elucidate whether the secular change in body proportions could explain the poor fit of the Japanese spirometry data to the GLI-2012 equations. This would have bearing on the use of prediction equations for all countries in which there are ongoing secular changes in body frame.

Data on FEV1 and FVC were obtained between January 2007 and December 2010 from 12 centers across Japan,11 using equipment (International Electrotechnical Commission [60601-1 and 60601-1-2] certified) and quality criteria that complied with international recommendations.14 Spirometric data from 20,336 healthy subjects (13,492 women) aged 17 to 95 years, height range 132 to 195 cm, were analyzed to derive national reference equations.11 Healthy subjects were lifelong nonsmokers with no evidence of respiratory disease or health conditions that might adversely affect pulmonary function.

To assess effects of changes in body proportions, we used annually published data on average standing height, sitting height, and weight of 5- to 17-year-old students from the Japanese Ministry of Education, Culture, Sports, Science and Technology (http://www.e-stat.go.jp/SG1/estat/List.do?bid=000001014499&). Every spring, a 4% to 5% stratified random sample of the total Japanese school population was investigated, with anthropometric measurements being performed with the same techniques during the period of data collection. Stadiometers with a movable right angle headpiece and an attached measuring tape (or electronic device) were used to measure height and sitting height. We extracted the average Cormic index of 17-year-old students from the annual reports for 1949 to 2012. This study is a retrospective analysis of data that have been deidentified, obviating the need for approval from local ethics committees.

The Japanese data for FEV1 and FVC were transformed to z scores based on the GLI-2012 prediction equations for Europeans1 using GLI software (http://www.lungfunction.org/tools.html). As the Cormic index did not change within Japanese birth cohorts between 13 and 17 years,13 we used the cohort-specific average Cormic index of 17-year-olds as representative of young adults. This allowed the spirometry to be adjusted for secular differences in the upper body segment, as described here.

Consider two subjects of the same height H with differing Cormic indexes x1 and x2, so that their sitting heights, representing the upper body segment, are in the ratio x1/x2, implying differing chest and lung volumes. In the GLI equations, FEV1 and FVC are predicted as power functions of height Hk, where the exponent k is given in Table 1. Thus, on the (admittedly extreme) assumption that the association of spirometry with height depends purely on the upper body segment, and that leg length plays no part, predicted spirometry in the two subjects will be in the ratio (x1/x2)k.

Table Graphic Jump Location
TABLE 1 ]  Average Cormic Index by Age (Y of Birth), Derived From Annual Cohort Studies in Japan, and Exponents k According to GLI-20121 of the Relationship Between Spirometry and Height (Hk)

See Materials and Methods section for explanation of cohort studies. GLI = Global Lung Function Initiative.

The mean Cormic index in Japanese subjects is higher at age 70 than at age 30 (Table 1). Corrected for differences in age and body frame, it follows that in men, predicted FVC should be
100[(0.54590.5342)2.411]=5.4% 
larger in a 70-year-old (Cormic index, 0.5459) than in a 30-year-old (Cormic index, 0.5342). The percentage difference can be approximated in terms of z scores by taking into account the average coefficient of variation over the current age range (13.6%); thus, a difference of 5.4% equates to a z-score difference of 5.4%/13.6% = 0.40 units.

Similarly, in women, FVC in a 70-year-old should be 5.1% larger than in a 30-year-old, corresponding to a difference in z score between 30- and 70-year-old Japanese of 0.38 units. These calculations ignore height lost because of spinal column shrinkage and therefore overestimate the Cormic index in the elderly. A very crude estimate of the effect of shrinkage can be made as follows. As arm span is unaffected by aging,15 one can use the cross-sectional relationship between arm span and height to estimate height loss from age 40 to 75 years as 0.8% in men and 1.3% in women.16 Attributing this height loss solely to the upper body segment, the Cormic index in a 70-year-old man would be 0.5422 instead of 0.5459, leading to a 3.7% larger FVC than in a 30-year-old Japanese, and the z score would be 0.27 units higher. Corresponding figures in a 70-year-old woman are 2.5% higher FVC and 0.18 higher z score.

Median height for the two sexes was estimated as a P-spline function in age, using the GAMLSS (Generalized Additive Models for Location, Scale, and Shape) package version 4.2-817 in the statistical software R, version 3.0.3 (R Foundation, http://www.r-project.org). The model with the lowest Schwarz Bayesian Criterion was selected.

On average, the GLI-2012 z scores for FEV1 and FVC over the entire age range were between 0.32 and 0.45 units lower than those for people of European descent, corresponding to a difference of 4.35% to 6.12%. However, they showed an age-related trend. The mean z scores for FEV1 and FVC rose steeply between 40 and 80 years of age (Fig 1), with a nadir at age 40 years (ie, those born in the 1970s). For those > 70 years of age (ie, born before World War II), the results were comparable with those of Europeans. Mean z scores increased from 30 and 70 years by approximately 0.7 units in both sexes.

Figure Jump LinkFigure 1 –  Mean differences of FEV1 and FVC between Japanese data and reference values for whites, expressed as z scores, in women and men.Grahic Jump Location

Median height in the same population increased by 12.8 cm in men and 15.4 cm in women for birth dates between 1920 and 1970 and then plateaued. The mean Cormic index in 17-year-old Japanese girls and boys rose slightly from 1932 to the early 1940s, then fell steeply until about 1965, and then rose again after 1980 (Fig 2). This pattern reflects changes in diet and socioeconomic conditions, which are known to affect relative leg length.6 Thus, in 2012 the Cormic index was highest for those aged 70 years and lowest for those aged 30 to 50 years, even when adjusted for estimated shrinkage of the vertebral column with age (see the Materials and Methods section).

Figure Jump LinkFigure 2 –  Average Cormic index in 17-y-old women and men recorded in successive birth cohorts from 1932 to 1995.Grahic Jump Location

Figure 3 converts the age-specific Cormic indexes to the corresponding FEV1 and FVC z-score differences between Japanese cohorts (as shown by the example in the Materials and Methods section), where the z-score origin is arbitrarily set at the lowest Cormic index, at ages 30 to 50 years. Thus, the values are higher below age 30 years and after age 50 years, similar in shape to the curves in Figure 1. The size of the effect, which is up to 0.4 z scores, is about one-half the range seen in Figure 1. Thus, variation in Cormic index could explain up to 50% of the age-specific variation in mean FEV1 and FVC z score.

Figure Jump LinkFigure 3 –  A, B, Difference (Δ) between Japanese birth cohorts in z score in predicted FEV1 (A) and FVC (B) in women and men arising from the secular change in the Cormic index, relative to the lowest sitting height/height ratio in 30- to 35-y-old subjects.Grahic Jump Location

The GLI has been successful in predicting spirometric volumes in various ethnic groups as functions of age and height. The GLI model allows ethnic groups to differ by incorporating an ethnic-group-specific multiplier, which provides residuals that are broadly independent of age or height. On average, predicted values are 4.4% to 6.1% lower in Japanese than in Europeans. This is compatible with the idea that Japan was populated by migration waves from northern and southern East Asia,18 where levels of pulmonary function are 1.5% to 4% and 8.4% to 11.4% lower than in Europeans, respectively.1 However, reference to the population mean is deceptive. Japanese data do not fit the GLI model, as there is a substantial trend in the deviations from predicted (Fig 1). This finding prompted the current study, which highlights a number of points. The first is that standing height is not an ideal proxy for lung size, as the relative contribution of sitting height to stature may differ between birth cohorts with the same ethnic origins, because of secular changes. The dimensions of the upper body segment, approximated by sitting height, should be a better proxy for lung size. Indeed, variation in Cormic index explains up to one-half of the differences in FEV1 and FVC between young and old Japanese subjects. Adjusting for the Cormic index has bearing only on chest height, not on chest depth and width, leaving the remaining differences in lung volumes between Japanese cohorts to be explained by other differences in chest geometry.

The secular trends in height and leg length in Japan are well documented and are linked to changes in the age at onset of maturation, changes in socioeconomic conditions, and adoption of a western life style.68,12,13,19 The increase in height has been due almost entirely to longer legs,12 so that sitting height has not materially altered. However, height stopped increasing after 1970, linked to the adoption of a more sedentary lifestyle and a change in diet,20 whereas, as shown in Figure 2, relative leg length started to decline after 1980, implying an absolute increase in sitting height. Thus, longer relative leg length at least partially explains why lung volumes are lowest, standardized for age and height, around age 40 years (Fig 1).

On average, adult Europeans have a lower Cormic index than Asians,21 varying between 0.513 (The Netherlands)22 and 0.525 (Poland)23; thus, for the same stature, Japanese subjects ought to have larger lungs, yet except for the elderly (Fig 1) with the highest Cormic index (Fig 2) they do not. This implies that differences in body frame independent of stature and sitting height, along with other genetic, epigenetic, or environmental factors, must account for lung volumes being larger in Europeans than Japanese.

Another lesson to be learned is that the scatter around predicted values can be partly explained by differences in body frame both within and between age cohorts. Subjects with a larger Cormic index can be expected to have systematically higher lung volumes than those of the same height with longer legs. This should be kept in mind when interpreting test results that are near the lower limit of normal, particularly in subjects with an unusual body habitus.

In subjects of European descent, the secular trend in height has stopped.7,22,2427 Therefore, in these ethnically homogeneous populations there is little to be gained by predicting lung volumes from sitting height rather than stature. However, in low-income countries, improving health conditions are likely to drive increases in height and changes in relative leg length. This implies that prediction equations for such populations will need to be periodically updated. Irrespective of current residence, the location where individuals were born and raised may make an important difference, since changes in body habitus are less likely to have occurred in poor rural areas than in wealthier urban ones. Such changes in body frame may also lead to differences in lung function between offspring of migrants to high-income countries compared with the country of origin.28 But it also applies to Japan, a highly developed and affluent country, because of its legacy of a falling Cormic index up to 1970 that will continue to bias predicted values for at least 40 years.

This study has strengths and limitations. Among the strengths is the fact that the spirometry data relate to a large population sample of healthy subjects aged 17 to 95 years, collected with standardized techniques and certified equipment, and subject to state-of-the art quality control. A weakness is that sitting height was not measured at time of spirometric measurements, and instead we used historic data on the Cormic index in 17-year-old subjects. Although not ideal, this is probably reasonable, as there was no change in the Cormic index within birth cohorts after age 13 years,13 as also seen in Dutch adolescents.22 After age 40 to 45 years, decalcification and compression of the trunk leads to a change in Cormic index that affects women more than men; as shown in the methods section, a crude approximation of the age-related shrinkage of the upper body segment reduces the secular trend in Cormic index in elderly subjects and reduces the age- and height-corrected difference in lung function between young and elderly Japanese adults.

We conclude that the GLI model for predicting spirometric lung volumes does not fit contemporary Japanese data, necessitating separate national reference values.11 Much of the deviation from predicted can be explained by secular changes in the Cormic index, leading to secular differences in FVC and FEV1. The magnitude of differences in the sitting height/standing height ratio between birth cohorts will necessitate periodic updates of reference equations for spirometry in the Japanese, at least every 20 years. This conclusion applies to any population in which the Cormic index shows a secular trend.

Author contributions: P. H. Q. is the guarantor. P. H. Q. contributed to the study concept, data analysis, and manuscript writing; M. Kubota contributed to the study concept, survey design and administration, data analysis, and manuscript writing; H. K. contributed to the study concept, survey design and administration, and review of the manuscript; H. O. and K. T. contributed to the data analysis, review of the manuscript, and survey design and administration; M. Kanazawa contributed to the study concept, survey design, and review of the manuscript; S. S. and T. J. C. contributed to the data analysis and manuscript writing and provided statistical expertise; and J. S. contributed to the data analysis and manuscript writing.

Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Other contributions: We thank the PFT Laboratory Directors at all participating Japanese institutions for their participation; we also thank the Japanese Respiratory Society for permission to use these data.

GLI

Global Lung Function Initiative

Quanjer PH, Stanojevic S, Cole TJ, et al; ERS Global Lung Function Initiative. Multi-ethnic reference values for spirometry for the 3-95-yr age range: the global lung function 2012 equations. Eur Respir J. 2012;40(6):1324-1343. [CrossRef] [PubMed]
 
West GB, Brown JH, Enquist BJ. A general model for the origin of allometric scaling laws in biology. Science. 1997;276(5309):122-126. [CrossRef] [PubMed]
 
Harik-Khan RI, Muller DC, Wise RA. Racial difference in lung function in African-American and White children: effect of anthropometric, socioeconomic, nutritional, and environmental factors. Am J Epidemiol. 2004;160(9):893-900. [CrossRef] [PubMed]
 
Harik-Khan RI, Fleg JL, Muller DC, Wise RA. The effect of anthropometric and socioeconomic factors on the racial difference in lung function. Am J Respir Crit Care Med. 2001;164(9):1647-1654. [CrossRef] [PubMed]
 
Whitrow MJ, Harding S. Ethnic differences in adolescent lung function: anthropometric, socioeconomic, and psychosocial factors. Am J Respir Crit Care Med. 2008;177(11):1262-1267. [CrossRef] [PubMed]
 
Cole TJ. Secular trends in growth. Proc Nutr Soc. 2000;59(2):317-324. [CrossRef] [PubMed]
 
Cole TJ. The secular trend in human physical growth: a biological view. Econ Hum Biol. 2003;1(2):161-168. [CrossRef] [PubMed]
 
Bogin B, Varela-Silva MI. Leg length, body proportion, and health: a review with a note on beauty. Int J Environ Res Public Health. 2010;7(3):1047-1075. [CrossRef] [PubMed]
 
Hall GL, Thompson BR, Stanojevic S, et al. The Global Lung Initiative 2012 reference values reflect contemporary Australasian spirometry. Respirology. 2012;17(7):1150-1151. [CrossRef] [PubMed]
 
Bonner R, Lum S, Stocks J, Kirkby J, Wade A, Sonnappa S. Applicability of the global lung function spirometry equations in contemporary multiethnic children. Am J Respir Crit Care Med. 2013;188(4):515-516. [CrossRef] [PubMed]
 
Kubota M, Kobayashi H, Quanjer PH, Omori H, Tatsumi K, Kanazawa M; Clinical Pulmonary Functions Committee of the Japanese Respiratory Society. Reference values for spirometry, including vital capacity, in Japanese adults calculated with the LMS method and compared with previous values. Respir Investig. 2014;52(4):242-250. [CrossRef] [PubMed]
 
Tanner JM, Hayashi T, Preece MA, Cameron N. Increase in length of leg relative to trunk in Japanese children and adults from 1957 to 1977: comparison with British and with Japanese Americans. Ann Hum Biol. 1982;9(5):411-423. [CrossRef] [PubMed]
 
Ali MA, Uetake T, Ohtsuki F. Secular changes in relative leg length in post-war Japan. Am J Hum Biol. 2000;12(3):405-416. [CrossRef] [PubMed]
 
Miller MR, Hankinson J, Brusasco V, et al; ATS/ERS Task Force. Standardisation of spirometry. Eur Respir J. 2005;26(2):319-338. [CrossRef] [PubMed]
 
van Leer EM, van Noord PA, Seidell JC. Components of adult height and height loss. Secular trend and effects of aging in women in the DOM project. Ann Epidemiol. 1992;2(5):611-615. [CrossRef] [PubMed]
 
Quanjer PH, Capderou A, Mazicioglu MM, et al. All-age relationship between arm span and height in different ethnic groups. Eur Respir J. 2014;44(4):905-912. [CrossRef] [PubMed]
 
Rigby RA, Stasinopoulos DM. Generalized additive models for location, scale and shape (with discussion). Appl Stat. 2005;54(3):507-554.
 
Nakaoka H, Mitsunaga S, Hosomichi K, et al. Detection of ancestry informative HLA alleles confirms the admixed origins of Japanese population. PLoS ONE. 2013;8(4):e60793. [CrossRef] [PubMed]
 
Tsuzaki S, Matsuo N, Ogata T, Osano M. Lack of linkage between height and weight and age at menarche during the secular shift in growth of Japanese children. Ann Hum Biol. 1989;16(5):429-436. [CrossRef] [PubMed]
 
Murata M. Secular trends in growth and changes in eating patterns of Japanese children. Am J Clin Nutr. 2000;72(suppl 5):1379S-1383S. [PubMed]
 
Eveleth PB, Tanner JM. Worldwide Variation in Human Growth. Cambridge, England: Cambridge University Press; 1976.
 
Fredriks AM, van Buuren S, van Heel WJM, Dijkman-Neerincx RH, Verloove-Vanhorick SP, Wit JM. Nationwide age references for sitting height, leg length, and sitting height/height ratio, and their diagnostic value for disproportionate growth disorders. Arch Dis Child. 2005;90(8):807-812. [CrossRef] [PubMed]
 
Grasgruber P, Hrazdíra E. Anthropometric characteristics of the young Czech population and their relationship to the national sports potential. Journal of Human Sport and Exercise. 2013;8(2):120. [CrossRef]
 
Larnkaer A, Attrup Schrøder S, Schmidt IM, Hørby Jørgensen M, Fleischer Michaelsen K. Secular change in adult stature has come to a halt in northern Europe and Italy. Acta Paediatr. 2006;95(6):754-755. [CrossRef] [PubMed]
 
Gohlke B, Woelfle J. Growth and puberty in German children: is there still a positive secular trend? Dtsch Arztebl Int. 2009;106(23):377-382. [PubMed]
 
Schönbeck Y, Talma H, van Dommelen P, et al. The world’s tallest nation has stopped growing taller: the height of Dutch children from 1955 to 2009. Pediatr Res. 2013;73(3):371-377. [CrossRef] [PubMed]
 
Smith SM, Craig LC, Raja AE, McNeill G, Turner SW. Growing up before growing out: secular trends in height, weight and obesity in 5--6-year-old children born between 1970 and 2006. Arch Dis Child. 2013;98(4):269-273. [CrossRef] [PubMed]
 
Fulambarker A, Copur AS, Cohen ME, et al. Comparison of pulmonary function in immigrant vs US-born Asian Indians. Chest. 2010;137(6):1398-1404. [CrossRef] [PubMed]
 

Figures

Figure Jump LinkFigure 1 –  Mean differences of FEV1 and FVC between Japanese data and reference values for whites, expressed as z scores, in women and men.Grahic Jump Location
Figure Jump LinkFigure 2 –  Average Cormic index in 17-y-old women and men recorded in successive birth cohorts from 1932 to 1995.Grahic Jump Location
Figure Jump LinkFigure 3 –  A, B, Difference (Δ) between Japanese birth cohorts in z score in predicted FEV1 (A) and FVC (B) in women and men arising from the secular change in the Cormic index, relative to the lowest sitting height/height ratio in 30- to 35-y-old subjects.Grahic Jump Location

Tables

Table Graphic Jump Location
TABLE 1 ]  Average Cormic Index by Age (Y of Birth), Derived From Annual Cohort Studies in Japan, and Exponents k According to GLI-20121 of the Relationship Between Spirometry and Height (Hk)

See Materials and Methods section for explanation of cohort studies. GLI = Global Lung Function Initiative.

References

Quanjer PH, Stanojevic S, Cole TJ, et al; ERS Global Lung Function Initiative. Multi-ethnic reference values for spirometry for the 3-95-yr age range: the global lung function 2012 equations. Eur Respir J. 2012;40(6):1324-1343. [CrossRef] [PubMed]
 
West GB, Brown JH, Enquist BJ. A general model for the origin of allometric scaling laws in biology. Science. 1997;276(5309):122-126. [CrossRef] [PubMed]
 
Harik-Khan RI, Muller DC, Wise RA. Racial difference in lung function in African-American and White children: effect of anthropometric, socioeconomic, nutritional, and environmental factors. Am J Epidemiol. 2004;160(9):893-900. [CrossRef] [PubMed]
 
Harik-Khan RI, Fleg JL, Muller DC, Wise RA. The effect of anthropometric and socioeconomic factors on the racial difference in lung function. Am J Respir Crit Care Med. 2001;164(9):1647-1654. [CrossRef] [PubMed]
 
Whitrow MJ, Harding S. Ethnic differences in adolescent lung function: anthropometric, socioeconomic, and psychosocial factors. Am J Respir Crit Care Med. 2008;177(11):1262-1267. [CrossRef] [PubMed]
 
Cole TJ. Secular trends in growth. Proc Nutr Soc. 2000;59(2):317-324. [CrossRef] [PubMed]
 
Cole TJ. The secular trend in human physical growth: a biological view. Econ Hum Biol. 2003;1(2):161-168. [CrossRef] [PubMed]
 
Bogin B, Varela-Silva MI. Leg length, body proportion, and health: a review with a note on beauty. Int J Environ Res Public Health. 2010;7(3):1047-1075. [CrossRef] [PubMed]
 
Hall GL, Thompson BR, Stanojevic S, et al. The Global Lung Initiative 2012 reference values reflect contemporary Australasian spirometry. Respirology. 2012;17(7):1150-1151. [CrossRef] [PubMed]
 
Bonner R, Lum S, Stocks J, Kirkby J, Wade A, Sonnappa S. Applicability of the global lung function spirometry equations in contemporary multiethnic children. Am J Respir Crit Care Med. 2013;188(4):515-516. [CrossRef] [PubMed]
 
Kubota M, Kobayashi H, Quanjer PH, Omori H, Tatsumi K, Kanazawa M; Clinical Pulmonary Functions Committee of the Japanese Respiratory Society. Reference values for spirometry, including vital capacity, in Japanese adults calculated with the LMS method and compared with previous values. Respir Investig. 2014;52(4):242-250. [CrossRef] [PubMed]
 
Tanner JM, Hayashi T, Preece MA, Cameron N. Increase in length of leg relative to trunk in Japanese children and adults from 1957 to 1977: comparison with British and with Japanese Americans. Ann Hum Biol. 1982;9(5):411-423. [CrossRef] [PubMed]
 
Ali MA, Uetake T, Ohtsuki F. Secular changes in relative leg length in post-war Japan. Am J Hum Biol. 2000;12(3):405-416. [CrossRef] [PubMed]
 
Miller MR, Hankinson J, Brusasco V, et al; ATS/ERS Task Force. Standardisation of spirometry. Eur Respir J. 2005;26(2):319-338. [CrossRef] [PubMed]
 
van Leer EM, van Noord PA, Seidell JC. Components of adult height and height loss. Secular trend and effects of aging in women in the DOM project. Ann Epidemiol. 1992;2(5):611-615. [CrossRef] [PubMed]
 
Quanjer PH, Capderou A, Mazicioglu MM, et al. All-age relationship between arm span and height in different ethnic groups. Eur Respir J. 2014;44(4):905-912. [CrossRef] [PubMed]
 
Rigby RA, Stasinopoulos DM. Generalized additive models for location, scale and shape (with discussion). Appl Stat. 2005;54(3):507-554.
 
Nakaoka H, Mitsunaga S, Hosomichi K, et al. Detection of ancestry informative HLA alleles confirms the admixed origins of Japanese population. PLoS ONE. 2013;8(4):e60793. [CrossRef] [PubMed]
 
Tsuzaki S, Matsuo N, Ogata T, Osano M. Lack of linkage between height and weight and age at menarche during the secular shift in growth of Japanese children. Ann Hum Biol. 1989;16(5):429-436. [CrossRef] [PubMed]
 
Murata M. Secular trends in growth and changes in eating patterns of Japanese children. Am J Clin Nutr. 2000;72(suppl 5):1379S-1383S. [PubMed]
 
Eveleth PB, Tanner JM. Worldwide Variation in Human Growth. Cambridge, England: Cambridge University Press; 1976.
 
Fredriks AM, van Buuren S, van Heel WJM, Dijkman-Neerincx RH, Verloove-Vanhorick SP, Wit JM. Nationwide age references for sitting height, leg length, and sitting height/height ratio, and their diagnostic value for disproportionate growth disorders. Arch Dis Child. 2005;90(8):807-812. [CrossRef] [PubMed]
 
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    Print ISSN: 0012-3692
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