Body fat mass distribution and interrupter resistance, fractional exhaled nitric oxide, and asthma at school-age

Journal of Allergy and Clinical Immunology

Volumn 139, Issue 3, 2017, Pages 810-818.e6

  den Dekker, Herman T ^a   Ros, Karen P I ^a   de Jongste, Johan C ^a   Reiss, Irwin K ^a   Jaddoe, Vincent W ^a   Duijts, Liesbeth ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

asthma; body composition; body fat mass distribution; fractional exhaled nitric oxide (FENO); Obesity; Rint; wheezing

Indexed keywords

NITRIC OXIDE;

ABDOMINAL SUBCUTANEOUS FAT; ARTICLE; ASTHMA; ATOPY; BODY FAT DISTRIBUTION; BODY MASS; CHILD; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DUAL ENERGY X RAY ABSORPTIOMETRY; FAT MASS; FEMALE; FOLLOW UP; HUMAN; LUNG FUNCTION; LUNG RESISTANCE; MAJOR CLINICAL STUDY; MALE; OBESITY; PHYSICAL EXAMINATION; POPULATION RESEARCH; PRESCHOOL CHILD; PRIORITY JOURNAL; PROSPECTIVE STUDY; ULTRASOUND; WHEEZING; ABNORMAL RESPIRATORY SOUND; ADIPOSE TISSUE; EXHALATION; METABOLISM; PATHOPHYSIOLOGY;

ADIPOSE TISSUE; ASTHMA; BODY MASS INDEX; CHILD; EXHALATION; FEMALE; HUMANS; MALE; NITRIC OXIDE; PROSPECTIVE STUDIES; RESPIRATORY SOUNDS;

EID: 85025078247     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2016.06.022     Document Type: Article

References (65)

1. Lai, C.K., Beasley, R., Crane, J., Foliaki, S., Shah, J., Weiland, S., Global variation in the prevalence and severity of asthma symptoms: phase three of the International Study of Asthma and Allergies in Childhood (ISAAC). Thorax 64 (2009), 476–483.
2. Kipping, R.R., Jago, R., Lawlor, D.A., Obesity in children, part 2: prevention and management. BMJ, 337, 2008, a1848.
3. Permaul, P., Kanchongkittiphon, W., Phipatanakul, W., Childhood asthma and obesity–what is the true link?. Ann Allergy Asthma Immunol 113 (2014), 244–246.
4. Guibas, G.V., Manios, Y., Xepapadaki, P., Moschonis, G., Douladiris, N., Mavrogianni, C., et al. The obesity-asthma link in different ages and the role of body mass index in its investigation: findings from the Genesis and Healthy Growth Studies. Allergy 68 (2013), 1298–1305.
5. Ashwell, M., Hsieh, S.D., Six reasons why the waist-to-height ratio is a rapid and effective global indicator for health risks of obesity and how its use could simplify the international public health message on obesity. Int J Food Sci Nutr 56 (2005), 303–307.
6. Gaggini, M., Saponaro, C., Gastaldelli, A., Not all fats are created equal: adipose vs. ectopic fat, implication in cardiometabolic diseases. Horm Mol Biol Clin Investig 22 (2015), 7–18.
7. Mook-Kanamori, D.O., Holzhauer, S., Hollestein, L.M., Durmus, B., Manniesing, R., Koek, M., et al. Abdominal fat in children measured by ultrasound and computed tomography. Ultrasound Med Biol 35 (2009), 1938–1946.
8. Holzhauer, S., Zwijsen, R.M., Jaddoe, V.W., Boehm, G., Moll, H.A., Mulder, P.G., et al. Sonographic assessment of abdominal fat distribution in infancy. Eur J Epidemiol 24 (2009), 521–529.
9. Kruithof, C.J., Kooijman, M.N., van Duijn, C.M., Franco, O.H., de Jongste, J.C., Klaver, C.C., et al. The Generation R Study: Biobank update 2015. Eur J Epidemiol 29 (2014), 911–927.
10. Kaul, S., Rothney, M.P., Peters, D.M., Wacker, W.K., Davis, C.E., Shapiro, M.D., et al. Dual-energy X-ray absorptiometry for quantification of visceral fat. Obesity (Silver Spring) 20 (2012), 1313–1318.
11. Helba, M., Binkovitz, L.A., Pediatric body composition analysis with dual-energy X-ray absorptiometry. Pediatr Radiol 39 (2009), 647–656.
12. World Health Organization. Nutrition, physical activity and obesity. 2013. Available at: http://www.euro.who.int/en/health-topics/disease-prevention/nutrition/country-work/netherlands. Accessed March 16, 2016.
13. American Thoracic Society, European Respiratory Society. ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide, 2005. Am J Respir Crit Care Med 171 (2005), 912–930.
14. Beydon, N., Davis, S.D., Lombardi, E., Allen, J.L., Arets, H.G., Aurora, P., et al. An official American Thoracic Society/European Respiratory Society statement: pulmonary function testing in preschool children. Am J Respir Crit Care Med 175 (2007), 1304–1345.
15. Merkus, P.J., Stocks, J., Beydon, N., Lombardi, E., Jones, M., McKenzie, S.A., et al. Reference ranges for interrupter resistance technique: the Asthma UK Initiative. Eur Respir J 36 (2010), 157–163.
16. Asher, M.I., Keil, U., Anderson, H.R., Beasley, R., Crane, J., Martinez, F., et al. International Study of Asthma and Allergies in Childhood (ISAAC): rationale and methods. Eur Respir J 8 (1995), 483–491.
17. De Beurs E. Brief Symptom Inventory, Handleiding Addendum. Leiden, The Netherlands: PITS BV, 2009.
18. Cole, T.J., Bellizzi, M.C., Flegal, K.M., Dietz, W.H., Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 320 (2000), 1240–1243.
19. Sterne, J.A., White, I.R., Carlin, J.B., Spratt, M., Royston, P., Kenward, M.G., et al. Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. BMJ, 338, 2009, b2393.
20. Cole, T.J., Sympercents: symmetric percentage differences on the 100 log(e) scale simplify the presentation of log transformed data. Stat Med 19 (2000), 3109–3125.
21. Egan, K.B., Ettinger, A.S., Bracken, M.B., Childhood body mass index and subsequent physician-diagnosed asthma: a systematic review and meta-analysis of prospective cohort studies. BMC Pediatr, 13, 2013, 121.
22. Weinmayr, G., Forastiere, F., Buchele, G., Jaensch, A., Strachan, D.P., Nagel, G., Overweight/obesity and respiratory and allergic disease in children: International Study of Asthma and Allergies in Childhood (ISAAC) phase two. PLoS One, 9, 2014, e113996.
23. Bekkers, M.B., Elstgeest, L.E., Scholtens, S., Haveman-Nies, A., de Jongste, J.C., Kerkhof, M., et al. Maternal use of folic acid supplements during pregnancy, and childhood respiratory health and atopy. Eur Respir J 39 (2012), 1468–1474.
24. Consilvio, N.P., Di Pillo, S., Verini, M., de Giorgis, T., Cingolani, A., Chiaveroli, V., et al. The reciprocal influences of asthma and obesity on lung function testing, AHR, and airway inflammation in prepubertal children. Pediatr Pulmonol 45 (2010), 1103–1110.
25. Tantisira, K.G., Litonjua, A.A., Weiss, S.T., Fuhlbrigge, A.L., Childhood Asthma Management Program Research Group. Association of body mass with pulmonary function in the Childhood Asthma Management Program (CAMP). Thorax 58 (2003), 1036–1041.
26. Han, Y.Y., Forno, E., Celedon, J.C., Adiposity, fractional exhaled nitric oxide, and asthma in U.S. children. Am J Respir Crit Care Med 190 (2014), 32–39.
27. Singleton, M.D., Sanderson, W.T., Mannino, D.M., Body mass index, asthma and exhaled nitric oxide in U.S. adults, 2007-2010. J Asthma 51 (2014), 756–761.
28. Fenger, R.V., Gonzalez-Quintela, A., Vidal, C., Gude, F., Husemoen, L.L., Aadahl, M., et al. Exploring the obesity-asthma link: do all types of adiposity increase the risk of asthma?. Clin Exp Allergy 42 (2012), 1237–1245.
29. Forno, E., Acosta-Perez, E., Brehm, J.M., Han, Y.Y., Alvarez, M., Colon-Semidey, A., et al. Obesity and adiposity indicators, asthma, and atopy in Puerto Rican children. J Allergy Clin Immunol 133 (2014), 1308–1314 1314.e1-5.
30. Chen, Y.C., Tu, Y.K., Huang, K.C., Chen, P.C., Chu, D.C., Lee, Y.L., Pathway from central obesity to childhood asthma: physical fitness and sedentary time are leading factors. Am J Respir Crit Care Med 189 (2014), 1194–1203.
31. Sideleva, O., Suratt, B.T., Black, K.E., Tharp, W.G., Pratley, R.E., Forgione, P., et al. Obesity and asthma: an inflammatory disease of adipose tissue not the airway. Am J Respir Crit Care Med 186 (2012), 598–605.
32. Lu, F.L., Johnston, R.A., Flynt, L., Theman, T.A., Terry, R.D., Schwartzman, I.N., et al. Increased pulmonary responses to acute ozone exposure in obese db/db mice. Am J Physiol Lung Cell Mol Physiol 290 (2006), L856–L865.
33. Shore, S.A., Terry, R.D., Flynt, L., Xu, A., Hug, C., Adiponectin attenuates allergen-induced airway inflammation and hyperresponsiveness in mice. J Allergy Clin Immunol 118 (2006), 389–395.
34. Salvi, S., Semper, A., Blomberg, A., Holloway, J., Jaffar, Z., Papi, A., et al. Interleukin-5 production by human airway epithelial cells. Am J Respir Cell Mol Biol 20 (1999), 984–991.
35. Yokoyama, A., Kohno, N., Fujino, S., Hamada, H., Inoue, Y., Fujioka, S., et al. Circulating interleukin-6 levels in patients with bronchial asthma. Am J Respir Crit Care Med 151 (1995), 1354–1358.
36. Arteaga-Solis, E., Zee, T., Emala, C.W., Vinson, C., Wess, J., Karsenty, G., Inhibition of leptin regulation of parasympathetic signaling as a cause of extreme body weight-associated asthma. Cell Metab 17 (2013), 35–48.
37. Altomonte, J., Harbaran, S., Richter, A., Dong, H., Fat depot-specific expression of adiponectin is impaired in Zucker fatty rats. Metabolism 52 (2003), 958–963.
38. Makki, K., Froguel, P., Wolowczuk, I., Adipose tissue in obesity-related inflammation and insulin resistance: cells, cytokines, and chemokines. ISRN Inflamm, 2013, 2013, 139239.
39. Calixto, M.C., Lintomen, L., Schenka, A., Saad, M.J., Zanesco, A., Antunes, E., Obesity enhances eosinophilic inflammation in a murine model of allergic asthma. Br J Pharmacol 159 (2010), 617–625.
40. Eising, J.B., Uiterwaal, C.S., Evelein, A.M., Visseren, F.L., van der Ent, C.K., Relationship between leptin and lung function in young healthy children. Eur Respir J 43 (2014), 1189–1192.
41. Lara, A., Khatri, S.B., Wang, Z., Comhair, S.A., Xu, W., Dweik, R.A., et al. Alterations of the arginine metabolome in asthma. Am J Respir Crit Care Med 178 (2008), 673–681.
42. Dweik, R.A., Boggs, P.B., Erzurum, S.C., Irvin, C.G., Leigh, M.W., Lundberg, J.O., et al. An official ATS clinical practice guideline: interpretation of exhaled nitric oxide levels (FENO) for clinical applications. Am J Respir Crit Care Med 184 (2011), 602–615.
43. Komakula, S., Khatri, S., Mermis, J., Savill, S., Haque, S., Rojas, M., et al. Body mass index is associated with reduced exhaled nitric oxide and higher exhaled 8-isoprostanes in asthmatics. Respir Res, 8, 2007, 32.
44. Berg, C.M., Thelle, D.S., Rosengren, A., Lissner, L., Toren, K., Olin, A.C., Decreased fraction of exhaled nitric oxide in obese subjects with asthma symptoms: data from the population study INTERGENE/ADONIX. Chest 139 (2011), 1109–1116.
45. Benson, R.C., Hardy, K.A., Morris, C.R., Arginase and arginine dysregulation in asthma. J Allergy (Cairo), 2011, 2011, 736319.
46. Einstein, F.H., Atzmon, G., Yang, X.M., Ma, X.H., Rincon, M., Rudin, E., et al. Differential responses of visceral and subcutaneous fat depots to nutrients. Diabetes 54 (2005), 672–678.
47. Kouda, K., Nakamura, H., Ohara, K., Fujita, Y., Iki, M., Increased ratio of trunk-to-appendicular fat and decreased adiponectin: a population-based study of school children in Hamamatsu, Japan. J Clin Densitom, 2015 Dec 2 pii: S1094-6950(15)00208-5.
48. Staiger, H., Tschritter, O., Machann, J., Thamer, C., Fritsche, A., Maerker, E., et al. Relationship of serum adiponectin and leptin concentrations with body fat distribution in humans. Obes Res 11 (2003), 368–372.
49. Farb, M.G., Ganley-Leal, L., Mott, M., Liang, Y., Ercan, B., Widlansky, M.E., et al. Arteriolar function in visceral adipose tissue is impaired in human obesity. Arterioscler Thromb Vasc Biol 32 (2012), 467–473.
50. Kujawska-Luczak, M., Suliburska, J., Markuszewski, L., Pupek-Musialik, D., Jablecka, A., Bogdanski, P., The effect of L-arginine and ascorbic acid on the visceral fat and the concentrations of metalloproteinases 2 and 9 in high-fat-diet rats. Endokrynol Pol 66 (2015), 526–532.
51. Miczke, A., Suliburska, J., Pupek-Musialik, D., Ostrowska, L., Jablencka, A., Kreipcio, Z., et al. Effect of L-arginine supplementation on insulin resistance and serum adiponectin concentration in rats with fat diet. Int J Clin Exp Med 8 (2015), 10358–10366.
52. Savgan-Gurol, E., Bredella, M., Russell, M., Mendes, N., Klibanski, A., Misra, M., Waist to hip ratio and trunk to extremity fat (DXA) are better surrogates for IMCL and for visceral fat respectively than for subcutaneous fat in adolescent girls. Nutr Metab (Lond), 7, 2010, 86.
53. Chan, D.C., Watts, G.F., Barrett, P.H., Burke, V., Waist circumference, waist-to-hip ratio and body mass index as predictors of adipose tissue compartments in men. QJM 96 (2003), 441–447.
54. Pouliot, M.C., Despres, J.P., Lemieux, S., Moorjani, S., Bouchard, C., Tremblay, A., et al. Waist circumference and abdominal sagittal diameter: best simple anthropometric indexes of abdominal visceral adipose tissue accumulation and related cardiovascular risk in men and women. Am J Cardiol 73 (1994), 460–468.
55. Delacourt, C., Lorino, H., Fuhrman, C., Herve-Guillot, M., Reinert, P., Harf, A., et al. Comparison of the forced oscillation technique and the interrupter technique for assessing airway obstruction and its reversibility in children. Am J Respir Crit Care Med 164 (2001), 965–972.
56. Beydon, N., M'Buila, C., Bados, A., Peiffer, C., Bernard, A., Zaccaria, I., et al. Interrupter resistance short-term repeatability and bronchodilator response in preschool children. Respir Med 101 (2007), 2482–2487.
57. Merkus, P.J., Mijnsbergen, J.Y., Hop, W.C., de Jongste, J.C., Interrupter resistance in preschool children: measurement characteristics and reference values. Am J Respir Crit Care Med 163 (2001), 1350–1355.
58. Klug, B., Bisgaard, H., Specific airway resistance, interrupter resistance, and respiratory impedance in healthy children aged 2-7 years. Pediatr Pulmonol 25 (1998), 322–331.
59. Turner, E.L., Dobson, J.E., Pocock, S.J., Categorisation of continuous risk factors in epidemiological publications: a survey of current practice. Epidemiol Perspect Innov, 7, 2010, 9.
60. Kaul, S., Rothney, M.P., Peters, D.M., Wacker, W.K., Davis, C.E., Shapiro, M.D., et al. Dual-energy X-ray absorptiometry for quantification of visceral fat. Obesity (Silver Spring) 20 (2012), 1313–1318.
61. Mook-Kanamori, D.O., Holzhauer, S., Hollestein, L.M., Durmus, B., Manniesing, R., Koek, M., et al. Abdominal fat in children measured by ultrasound and computed tomography. Ultrasound Med Biol 35 (2009), 1938–1946.
62. Suzuki, R., Watanabe, S., Hirai, Y., Akiyama, K., Nishide, T., Matsushima, Y., et al. Abdominal wall fat index, estimated by ultrasonography, for assessment of the ratio of visceral fat to subcutaneous fat in the abdomen. Am J Med 95 (1993), 309–314.
63. Beydon, N., Davis, S.D., Lombardi, E., Allen, J.L., Arets, H.G., Aurora, P., et al. American Thoracic Society/European Respiratory Society Working Group on I, Young Children Pulmonary Function T. An official American Thoracic Society/European Respiratory Society statement: pulmonary function testing in preschool children. Am J Respir Crit Care Med 175 (2007), 1304–1345.
64. American Thoracic Society, European Respiratory Society. ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide, 2005. Am J Respir Crit Care Med 171 (2005), 912–930.
65. Sterne, J.A., White, I.R., Carlin, J.B., Spratt, M., Royston, P., Kenward, M.G., et al. Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. BMJ, 338, 2009, b2393.