Influence of sex, age, pubertal maturation and body mass index on circulating white blood cell counts in healthy European adolescents—the HELENA study

European Journal of Pediatrics

Volumn 174, Issue 8, 2015, Pages 999-1014

  Pérez de Heredia, Fátima ^a,b   Gómez Martínez, Sonia ^b   Díaz, Ligia Esperanza ^b   Veses, Ana M ^b   Nova, Esther ^b   Wärnberg, Julia ^c   Huybrechts, Inge ^d,e   Vyncke, Krishna ^d   Androutsos, Odysseas ^f   Ferrari, Marika ^g   Palacios, Gonzalo ^h   Wastlund, Acki ^c   Kovács, Éva ^i,j   Gottrand, Frédéric ^k   González Gross, Marcela ^h,l   Castillo, Manuel J ^m   Sjöstrom, Michael ^c   Manios, Yannis ^f   Kafatos, Anthony ⁿ   Molnár, Denes ⁱ   Widhalm, Kurt ^o   Moreno, Luis A ^p   Marcos, Ascensión ^b   more..

^a LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

^b INSTITUTE OF FOOD SCIENCE   (Spain)

^c KAROLINSKA INSTITUTE   (Sweden)

^d GHENT UNIVERSITY   (Belgium)

^e INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^f HAROKOPIO UNIVERSITY   (Greece)

^g ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^h UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

ⁱ UNIVERSITY OF PÉCS   (Hungary)

^j UNIVERSITY OF MUNICH   (Germany)

^k UNIVERSITÉ DE LILLE   (France)

^l UNIVERSITY OF BONN   (Germany)

^m UNIVERSITY OF GRANADA   (Spain)

ⁿ UNIVERSITY OF CRETE   (Greece)

^o UNIVERSITY OF SALZBURG   (Austria)

^p UNIVERSITY OF ZARAGOZA   (Spain)

more..

Author keywords

Adolescents; Body mass index; Immune cells; Immunophenotyping; Puberty; Sex

Indexed keywords

CD16 ANTIGEN; CD19 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD45RA ANTIGEN; CD45RO ANTIGEN; CD56 ANTIGEN; CD8 ANTIGEN;

ADOLESCENT; AGE; ARTICLE; BASOPHIL; BODY MASS; CHILD; EOSINOPHIL; EUROPEAN; FEMALE; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IMMUNOCOMPETENT CELL; IMMUNOPHENOTYPING; LEUKOCYTE COUNT; LYMPHOCYTE COUNT; MALE; MONOCYTE; MULTICENTER STUDY (TOPIC); NEUTROPHIL COUNT; NORMAL HUMAN; PRIORITY JOURNAL; PUBERTY; SEX DIFFERENCE; BLOOD; CLASSIFICATION; CYTOLOGY; LEUKOCYTE; LYMPHOCYTE; NEUTROPHIL; PHYSIOLOGY; REFERENCE VALUE; SEXUAL MATURATION;

ADOLESCENT; AGE FACTORS; BASOPHILS; BODY MASS INDEX; EOSINOPHILS; FEMALE; HUMANS; LEUKOCYTE COUNT; LEUKOCYTES; LYMPHOCYTES; MALE; MONOCYTES; NEUTROPHILS; PUBERTY; REFERENCE VALUES; SEX FACTORS; SEXUAL MATURATION;

EID: 84938289741     PISSN: 03406199     EISSN: 14321076     Source Type: Journal    
DOI: 10.1007/s00431-015-2497-5     Document Type: Article

References (38)

1. Friedman GD, Klatsky AL, Siegelaub AB (1974) The leukocyte count as a predictor of myocardial infarction. N Engl J Med 290:1275–1278. doi:10.1056/NEJM197406062902302
2. Scrimshaw NS (2007) Immunonutrition in health and disease. Br J Nutr 98(Suppl 1):S3–S4. doi:10.1017/S0007114507833034
3. Ford ES (2003) The metabolic syndrome and C-reactive protein, fibrinogen, and leukocyte count: findings from the Third National Health and Nutrition Examination Survey. Atherosclerosis 168:351–358. doi:10.1016/S0021-9150(03)00134-5
4. Ohshita K, Yamane K, Hanafusa M, Mori H, Mito K, Okubo M, Hara H, Kohno N (2004) Elevated white blood cell count in subjects with impaired glucose tolerance. Diabetes Care 27(2):491–496. doi:10.2337/diacare.27.2.491
5. Capuano V, Bambacaro A, Darminio T, Mazzot G (2001) White blood cell count is related to arterial pressure and cholesterolemia in normal children. Ital Heart J 2(9):685–689
6. Wu CZ, Hsiao FC, Lin JD, Su CC, Wang KS, Chu YM, Lee LH, Wang K, Hsia TL, Pei D (2010) Relationship between white blood cell count and components of the metabolic syndrome among young adolescents. Acta Diabetol 47:65–71. doi:10.1007/s00592-009-0101-z
7. Bartlett JA, Schleifer SJ, Demetrikopoulos MK, Delaney BR, Shiflett SC, Keller SE (1998) Immune function in healthy adolescents. Clin Diagn Lab Immunol 5:105–113
8. Cheng CK, Chan J, Cembrowski GS, van Assendelft OW (2004) Complete blood count reference interval diagrams derived from NHANES III: stratification by age, sex, and race. Lab Hematol 10(1):42–53
9. Comans-Bitter WM, de Groot R, van den Beemd R, Neijens HJ, Hop WCJ, Groeneveld K, Hooijkaas H, van Dongen JJM (1997) Immunophenotyping of blood lymphocytes in childhood. J Pediatr 130:388–393. doi:10.1016/S0022-3476(97)70200-2
10. Heldrup J, Kalm O, Prellner K (1992) Blood T and B lymphocyte subpopulations in healthy infants and children. Acta Paediatr 81(2):125–132
11. Huenecke S, Behl M, Fadler C, Zimmermann SY, Bochennek K, Tramsen L, Esser R, Klarmann D, Kamper M, Sattler A, von Laer D, Klingebiel T, Lehrnbecher T, Koehl U (2008) Age-matched lymphocyte subpopulation reference values in childhood and adolescence: application of exponential regression analysis. Eur J Haematol 80:532–539. doi:10.1111/j.1600-0609.2008.01052.x
12. Lin SC, Chou CC, Tsai MJ, Wu KH, Huang MT, Wang LH, Chiang BL (1998) Age-related changes in blood lymphocyte subsets of Chinese children. Pediatr Allergy Immunol 9(4):215–220
13. Rudy BJ, Wilson CM, Durako S, Moscicki AB, Muenz L, Douglas SD (2002) Peripheral blood lymphocyte subsets in adolescents: a longitudinal analysis from the REACH project. Clin Diagn Lab Immunol 9(5):959–965. doi:10.1128%2FCDLI.9.5.959-965.2002
14. Shearer WT, Rosenblatt HM, Gelman RS, Oyomopito R, Plaeger S, Stiehm ER, Wara DW, Douglas SD, Luzuriaga K, McFarland EJ, Yogev R, Rathore MH, Levy W, Graham BL, Spector S, Pediatric AIDS Clinical Trials Group (2003) Lymphocyte subsets in healthy children from birth through 18 years of age: the Pediatric AIDS Clinical Trials Group P1009 study. J Allergy Clin Immunol 112:973–980. doi:10.1016/j.jaci.2003.07.003
15. Tollerud DJ, Ildstad ST, Brown LM, Clark JW, Blattner WA, Mann DL, Neuland CY, Pankiw-Trost L, Hoover RN (1990) T-cell subsets in healthy teenagers: transition to the adult phenotype. Clin Immunol Immunopathol 56(1):88–96
16. Bunders M, Cortina-Borja M, Newell ML, European Collaborative Study (2005) Age-related standards for total lymphocyte, CD4+ and CD8+ T cell counts in children born in Europe. Pediatr Infect Dis J 24(7):595–600
17. Choong ML, Ton SH, Cheong SK (1995) Influence of race, age and sex on the lymphocyte subsets in peripheral blood of healthy Malaysian adults. Ann Clin Biochem 32(6):532–539
18. Lim EM, Cembrowski G, Cembrowski M, Clarke G (2010) Race-specific WBC and neutrophil count reference intervals. Int J Lab Hematol 32(6):590–597. doi:10.1111/j.1751-553X.2010.01223.x
19. Santagostino A, Gargaccio G, Pistorio A, Bolis V, Camisasca G, Pagliaro P, Girotto M (1999) An Italian national multicenter study for the definition of a reference ranges for normal values of peripheral blood lymphocyte subsets in healthy adults. Haematologica 84:499–504
20. Zeh C, Amornkul PN, Inzaule S, Ondoa P, Oyaro B, Mwaengo DM, Vandenhoudt H, Gichangi A, Williamson J, Thomas T, Decock KM, Hart C, Nkengasong J, Laserson K (2011) Population-based biochemistry, immunologic and hematological reference values for adolescents and young adults in a rural population in Western Kenya. PLoS One 6(6):e21040. doi:10.1371/journal.pone.0021040
21. Moreno LA, González-Gross M, Kersting M, Molnár D, De Henauw S, Béghin L, Sjöström M, Hagströmer M, Manios Y, Gilbert CC, Ortega FB, Dallongeville J, Arcella D, Wärnberg J, Hallberg M, Fredriksson H, Maes L, Widhalm K, Kafatos AG, Marcos A (2008) Assessing, understanding and modifying nutritional status, eating habits and physical activity in European adolescents: the HELENA (Healthy Lifestyle in Europe by Nutrition in Adolescence) Study. Public Health Nutr 11(3):288–299. doi:10.1017/S1368980007000535
22. Moreno LA, De Henauw S, González-Gross M, Kersting M, Molnár D, Gottrand F, Barrios L, Sjöström M, Manios Y, Gilbert CC, Leclercq C, Widhalm K, Kafatos A, Marcos A, on behalf of the HELENA Study Group (2008) Design and implementation of the Health Lifestyle in Europe by Nutrition in Adolescence Cross-Sectional Study. Int J Obes 32:S4–S11. doi:10.1038/ijo.2008.177
23. Béghin L, Castera M, Manios Y, Gilbert CC, Kersting M, De Henauw S, Kafatos A, Gottrand F, Molnar D, Sjöström M, Leclercq C, Widhalm K, Mesana MI, Moreno LA, Libersa C, on behalf of the HELENA Study Group (2008) Quality assurance of ethical issues and regulatory aspects relating to good practices in the HELENA Cross-Sectional Study. Int J Obes 32:S12–S18. doi:10.1038/ijo.2008.179
24. Tanner JM, Whitehouse RH (1976) Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Arch Dis Child 51:170–179
25. Nagy E, Vicente-Rodriguez G, Manios Y, Beghin L, Iliescu C, Censi L, Dietrich S, Ortega Porcel FB, De Vriendt T, Plada M, Moreno LA, Molnar D, the HELENA Study Group (2008) Harmonization process and reliability assessment of anthropometric measurements in a multicenter study in adolescents. Int J Obes 32:S58–S65. doi:10.1038/ijo.2008.184
26. González-Gross M, Breidenassel C, Gómez-Martínez S, Ferrari M, Béghin L, Spinneker A, Díaz LE, Maiani G, Demailly A, Al-Tahan J, Albers U, Wärnberg J, Stoffel-Wagner B, Jiménez-Pavón D, Libersa C, Pietrzik K, Marcos A, Stehle P, the HELENA Study Group (2008) Sampling and processing of fresh blood samples within a European multicenter nutritional study: evaluation of biomarker stability during transport and storage. Int J Obes 32:S66–S75. doi:10.1038/ijo.2008.185
27. Romeo J, Wärnberg J, Gómez-Martínez S, Díaz LE, Moreno LA, Castillo MJ, Redondo C, Baraza JC, Sola R, Zamora S, Marcos A, on behalf of the AVENA group (2009) Haematological reference values in Spanish adolescents: the AVENA study. Eur J Haematol 83:586–594. doi:10.1111/j.1600-0609.2009.01326.x
28. Grossman C (1989) Possible underlying mechanisms of sexual dimorphism in the immune response, fact and hypothesis. J Steroid Biochem 34:241–251
29. Verthelyi D (2001) Sex hormones as immunomodulators in health and disease. Int Immunopharmacol 1:983–993. doi:10.1016/S1567-5769(01)00044-3
30. Brand JS, van der Schouw YT, Dowsett M, Folkerd E, Luben RN, Wareham NJ, Khaw KT (2012) Testosterone, SHBG and differential white blood cell count in middle-aged and older men. Maturitas 71(3):274–278. doi:10.1016/j.maturitas.2011.12.007
31. Schooling CM (2013) Androgen activity and markers of inflammation among men in NHANES III. Am J Hum Biol 25(5):622–628. doi:10.1002/ajhb.22421
32. Marcos A, Nova E, Montero A (2003) Changes in the immune system are conditioned by nutrition. Eur J Clin Nutr 57(Suppl 1):S66–S69. doi:10.1038/sj.ejcn.1601819
33. Pérez de Heredia F, Gómez-Martínez S, Marcos A (2012) Obesity, inflammation and the immune system. Proc Nutr Soc 71:332–338. doi:10.1017/S0029665112000092
34. Huang ZS, Chien KL, Yang CY, Tsai KS, Wang CH (2001) Peripheral differential leukocyte counts in humans vary with hyperlipidemia, smoking, and body mass index. Lipids 36(3):237–245
35. Hsieh CH, Pei D, Kuo SW, Chen CY, Tsai SL, Lai CL, Lee CH, Wu CZ, Hung YJ, Hsieh MC (2007) Correlation between white blood cell count and metabolic syndrome in adolescence. Pediatr Int 49(6):827–832. doi:10.1111/j.1442-200X.2007.02450.x
36. Zaldivar F, McMurray RG, Nemet D, Galassetti P, Mills PJ, Cooper DM (2006) Body fat and circulating leukocytes in children. Int J Obes (Lond) 30(6):906–911. doi:10.1038/sj.ijo.0803227
37. Nagasawa N, Tamakoshi K, Yatsuya H, Hori Y, Ishikawa M, Murata C, Zhang H, Wada K, Otsuka R, Mabuchi T, Kondo T, Toyoshima H (2004) Association of white blood cell count and clustered components of metabolic syndrome in Japanese men. Circ J 68(10):892–897. doi:10.1253/circj.68.892
38. Odagiri K, Uehara A, Mizuta I, Yamamoto M, Kurata C (2011) Longitudinal study on white blood cell count and the incidence of metabolic syndrome. Intern Med 50:2491–2498. doi:10.2169/internalmedicine.50.5877