Dimensions of socioeconomic status and childhood asthma outcomes: Evidence for distinct behavioral and biological associations

Psychosomatic Medicine

Volumn 78, Issue 9, 2016, Pages 1043-1052

  Chen, Edith ^a   Shalowitz, Madeleine U ^b   Story, Rachel E ^b   Ehrlich, Katherine B ^a   Levine, Cynthia S ^a   Hayen, Robin ^a   Leigh, Adam K K ^a   Miller, Gregory E ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHSHORE UNIVERSITY HEALTHSYSTEM   (United States)

Author keywords

asthma; childhood; immune; socioeconomic status

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5;

ADOLESCENT; ARTICLE; ASTHMA; CHILD; CLINICAL OUTCOME; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; ENVIRONMENTAL EXPOSURE; FEMALE; HEALTH BEHAVIOR; HOME ENVIRONMENT; HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; LUNG FUNCTION; MAJOR CLINICAL STUDY; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROVOCATION TEST; SMOKE; SOCIAL STATUS; SPIROMETRY; TH1 CELL; TH2 CELL; BLOOD; EDUCATIONAL STATUS; IMMUNOLOGY; INCOME; SOCIAL CLASS; STATISTICS AND NUMERICAL DATA;

ADOLESCENT; ASTHMA; CHILD; EDUCATIONAL STATUS; FEMALE; HEALTH BEHAVIOR; HUMANS; INCOME; MALE; SOCIAL CLASS;

EID: 84991447104     PISSN: 00333174     EISSN: 15347796     Source Type: Journal    
DOI: 10.1097/PSY.0000000000000392     Document Type: Article

References (78)

1. Miller GE Chen E Parker KJ. Psychological stress in childhood and susceptibility to the chronic diseases of aging: moving toward a model of behavioral and biological mechanisms. Psychol Bull 2011; 137: 959-97.
2. Galobardes B Lynch JW Smith GD. Childhood socioeconomic circumstances and cause-specific mortality in adulthood: systematic review and interpretation. Epidemiol Rev 2004; 26: 7-21.
3. Kuh D Hardy R Langenberg C Richards M Wadsworth ME. Mortality in adults aged 26-54 years related to socioeconomic conditions in childhood and adulthood: Post war birth cohort study. BMJ 2002; 325: 1076-80.
4. Kittleson MM Meoni LA Wang NY Chu AY Ford DE Klag MJ. Association of childhood socioeconomic status with subsequent coronary heart disease in physicians. Arch Intern Med 2006; 166: 2356-61.
5. Starfield B Riley AW Witt WP Robertson J. Social class gradients in health during adolescence. J Epidemiol Community Health 2002; 56: 354-61.
6. Chen E Matthews KA Boyce WT. Socioeconomic differences in children's health: How and why do these relationships change with age? Psychol Bull 2002; 128: 295-329.
7. Goodman E. The role of socioeconomic status gradients in explaining differences in US adolescents' health. Am J Public Health 1999; 89: 1522-8.
8. Marmot M Wilkinson RG. Social determinants of health, New York, NY: Oxford University Press; 2000.
9. Adler NE Rehkopf DH. U.S. disparities in health: descriptions, causes, and mechanisms. Annu Rev Public Health 2008; 29: 235-52.
10. Council NR. Cells and Surveys: Should Biological Measures be Included in Social Science Research?, Washington DC: The National Academies Press; 2001.
11. McDade TW Hayward MD. Rationale and methodological options for assessing infectious disease and related measures in social science surveys. Biodemography Soc Biol 2009; 55: 159-77.
12. Cohen S Doyle WJ Baum A. Socioeconomic status is associated with stress hormones. Psychosom Med 2006; 68: 414-20.
13. Cohen S Schwartz JE Epel E Kirschbaum C Sidney S Seeman T. Socioeconomic status, race, and diurnal cortisol decline in the Coronary Artery Risk Development in Young Adults (CARDIA) Study. Psychosom Med 2006; 68: 41-50.
14. Janicki-Deverts D Cohen S Adler NE Schwartz JE Matthews KA Seeman TE. Socioeconomic status is related to urinary catecholamines in the Coronary Artery Risk Development in Young Adults (CARDIA) study. Psychosom Med 2007; 69: 514-20.
15. Phillips JE Marsland AL Flory JD Muldoon MF Cohen S Manuck SB. Parental education is related to C-reactive protein among female middle-aged community volunteers. Brain Behav Immun 2009; 23: 677-83.
16. Friedman EM Herd P. Income, education, and inflammation: differential associations in a national probability sample (The MIDUS study). Psychosom Med 2010; 72: 290-300.
17. Deverts DJ Cohen S Kalra P Matthews KA. The prospective association of socioeconomic status with C-reactive protein levels in the CARDIA study. Brain Behav Immun 2012; 26: 1128-35.
18. Miller GE Lachman ME Chen E Gruenewald TL Seeman TE. Pathways to resilience: Maternal nurturance as a buffer against childhood poverty's effects on metabolic syndrome at midlife. Psychol Sci 2011; 22: 1591-9.
19. Taylor SE Lehman BJ Kiefe CI Seeman TE. Relationship of early life stress and psychological functioning to adult C-reactive protein in the Coronary Artery Risk Development in Young Adults Study. Biol Psychiatry 2006; 60: 819-24.
20. Danese A Moffitt TE Harrington H Milne BJ Polanczyk G Pariante CM Poulton R Caspi A. Adverse childhood experiences and adult risk factors for age-related disease: depression, inflammation, and clustering of metabolic risk markers. Arch Pediatr Adolesc Med 2009; 163: 1135-43.
21. Miller GE Chen E Fok AK Walker H Lim A Nicholls EF Cole S Kobor MS. Low early-life social class leaves a biological residue manifested by decreased glucocorticoid and increased proinflammatory signaling. Proc Natl Acad Sci U S A 2009; 106: 14716-21.
22. Ranjit N Diez-Roux AV Shea S Cushman M Ni H Seeman T. Socioeconomic position, race/ethnicity, and inflammation in the multi-ethnic study of atherosclerosis. Circulation 2007; 116: 2383-90.
23. Alley DE Seeman TE Ki Kim J Karlamangla A Hu P Crimmins EM. Socioeconomic status and C-reactive protein levels in the US population: NHANES IV. Brain Behav Immun 2006; 20: 498-504.
24. Matthews KA Chang Y Bromberger JT Karvonen-Gutierrez CA Kravitz HM Thurston RC Montez JK. Childhood socioeconomic circumstances, inflammation, and hemostasis among midlife women: Study of Women's Health Across the Nation. Psychosom Med 2016; 78: 311-8.
25. Friedman EM Karlamangla AS Gruenewald TL Koretz B Seeman TE. Early life adversity and adult biological risk profiles. Psychosom Med 2015; 77: 176-85.
26. Shonkoff JP Boyce WT McEwen BS. Neuroscience, molecular biology, and the childhood roots of health disparities: building a new framework for health promotion and disease prevention. JAMA 2009; 301: 2252-9.
27. Goodman E McEwen BS Huang B Dolan LM Adler NE. Social inequalities in biomarkers of cardiovascular risk in adolescence. Psychosom Med 2005; 67: 9-15.
28. Goodman E Daniels SR Dolan LM. Socioeconomic disparities in insulin resistance: Results from the Princeton School District Study. Psychosom Med 2007; 69: 61-7.
29. Thurston RC Matthews KA. Racial and socioeconomic disparities in arterial stiffness and intima media thickness among adolescents. Soc Sci Med 2009; 68: 807-13.
30. Burford TI Low CA Matthews KA. Night/day ratios of ambulatory blood pressure among healthy adolescents: roles of race, socioeconomic status, and psychosocial factors. Ann Behav Med 2013; 46: 217-26.
31. Miller G Chen E Cole SW. Health psychology: developing biologically plausible models linking the social world and physical health. Annu Rev Psychol 2009; 60: 501-24.
32. Busse WW Lemanske RF. Advances in immunology: asthma. N Engl J Med 2001; 344: 350-62.
33. Chung KF Barnes PJ. Cytokines in asthma. Thorax 1999; 54: 825-57.
34. Spellberg B Edwards JE. Type 1 type 2 immunity in infectious diseases. Clin Infect Dis 2001; 32: 76-102.
35. Mestas J Hughes CC. Of mice and not men: differences between mouse and human immunology. J Immunol 2004; 172: 2731-8.
36. Kang DH Fox C. Th1 and Th2 cytokine responses to academic stress. Res Nurs Health 2001; 24: 245-57.
37. Marshall GD Agarwal SK Lloyd C Cohen L Henninger EM Morris GJ. Cytokine dysregulation associated with exam stress in healthy medical students. Brain Behav Immun 1998; 12: 297-307.
38. Kang DH Coe CL McCarthy DO Jarjour NN Kelly EA Rodriguez RR Busse WW. Cytokine profiles of stimulated blood lymphocytes in asthmatic and healthy adolescents across the school year. J Interferon Cytokine Res 1997; 17: 481-7.
39. Chen E Hanson MD Paterson LQ Griffin MJ Walker HA Miller GE. Socioeconomic status and inflammatory processes in childhood asthma: the role of psychological stress. J Allergy Clin Immunol 2006; 117: 1014-20.
40. Chen E Fisher EB Bacharier LB Strunk RC. Socioeconomic status, stress, and immune markers in adolescents with asthma. Psychosom Med 2003; 65: 984-92.
41. Marin TJ Chen E Munch JA Miller GE. Double-exposure to acute stress and chronic family stress is associated with immune changes in children with asthma. Psychosom Med 2009; 71: 378-84.
42. Wright RJ Finn P Contreras JP Cohen S Wright RO Staudenmayer J Wand M Perkins D Weiss ST Gold DR. Chronic caregiver stress and IgE expression, allergen-induced proliferation, and cytokine profiles in a birth cohort predisposed to atopy. J Allergy Clin Immunol 2004; 113: 1051-7.
43. Wright RJ Visness CM Calatroni A Grayson MH Gold DR Sandel MT Lee-Parritz A Wood RA Kattan M Bloomberg GR Burger M Togias A Witter FR Sperling RS Sadovsky Y Gern JE. Prenatal maternal stress and cord blood innate and adaptive cytokine responses in an inner-city cohort. Am J Respir Crit Care Med 2010; 182: 25-33.
44. Simpson JL Brooks C Douwes J. Innate immunity in asthma. Paediatr Respir Rev 2008; 9: 263-70.
45. Finn PW Bigby TD. Innate immunity and asthma. Proc Am Thorac Soc 2009; 6: 260-5.
46. Jackson DJ Gangnon RE Evans MD Roberg KA Anderson EL Pappas TE Printz MC Lee WM Shult PA Reisdorf E Carlson-Dakes KT Salazar LP DaSilva DF Tisler CJ Gern JE Lemanske RF. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am J Respir Crit Care Med 2008; 178: 667-72.
47. Sigurs N Gustafsson PM Bjarnason R Lundberg F Schmidt S Sigurbergsson F Kjellman B. Severe respiratory syncytial virus bronchiolitis in infancy and asthma and allergy at age 13. Am J Respir Crit Care Med 2005; 171: 137-41.
48. Busillo JM Cidlowski JA. The five Rs of glucocorticoid action during inflammation: ready, reinforce, repress, resolve, and restore. Trends Endocrinol Metab 2013; 24: 109-19.
49. Miller GE Gaudin A Zysk E Chen E. Parental support and cytokine activity in childhood asthma: the role of glucocorticoid sensitivity. J Allergy Clin Immunol 2009; 128: 970-6.
50. Miller GE Chen E. Harsh family climate in early life presages the emergence of a proinflammatory phenotype in adolescence. Psychol Sci 2010; 21: 848-56.
51. Rohleder N Marin TJ Ma R Miller GE. Biologic cost of caring for a cancer patient: dysregulation of pro- and anti-inflammatory signaling pathways. J Clin Oncol 2009; 27: 2909-15.
52. Cohen S Janicki-Deverts D Doyle WJ Miller GE Frank E Rabin BS Turner RB. Chronic stress, glucocorticoid receptor resistance, inflammation, and disease risk. Proc Natl Acad Sci U S A 2012; 109: 5995-9.
53. Braveman PA Cubbin C Egerter S Chideya S Marchi KS Metzler M Posner S. Socioeconomic status in health research: one size does not fit all. JAMA 2005; 294: 2879-88.
54. Krieger N Williams DR Moss NE. Measuring social class in US public health research: Concepts, methodologies, and guidelines. Annu Rev Public Health 1997; 18: 341-78.
55. Bradley RH Corwyn RF. Socioeconomic status and child development. Annu Rev Psychol 2002; 53: 371-99.
56. Bornstein MH Bradley RH. Socioeconomic status, parenting, and child development, New York, NY: Routledge; 2014.
57. Winkleby MA Jatulis DE Frank E Fortmann SP. Socioeconomic status and health: how education, income, and occupation contribute to risk factors for cardiovascular disease. Am J Public Health 1992; 82: 816-20.
58. Herd P Goesling B House JS. Socioeconomic position and health: the differential effects of education versus income on the onset versus progression of health problems. J Health Soc Behav 2007; 48: 223-38.
59. Davis-Kean PE. The influence of parent education and family income on child achievement: the indirect role of parental expectations and the home environment. J Fam Psychol 2005; 19: 294-304.
60. Chen E Cohen S Miller GE. How low socioeconomic status affects 2-year hormonal trajectories in children. Psychol Sci 2010; 21: 31-7.
61. Corrigan CJ Kay AB. CD4 T-lymphocyte activation in acute severe asthma: Relationship to disease severity and atopic status. Am Rev Respir Dis 1990; 141: 970-7.
62. Gemou-Engesëth V Kay AB Bush A Corrigan CJ. Activated peripheral blood CD4 and CD8 T-lymphocytes in child asthma: correlation with eosinophilia and disease severity. Pediatr Allergy Immunol 1994; 5: 170-7.
63. Rosenblum Lichtenstein JH Hsu YH Gavin IM Donaghey TC Molina RM Thompson KJ Chi CL Gillis BS Brain JD. Environmental mold and mycotoxin exposures elicit specific cytokine and chemokine responses. PLoS One 2015; 10: e0126926.
64. Chowdhury F Williams A Johnson P. Validation and comparison of two multiplex technologies, Luminex and Mesoscale Discovery, for human cytokine profiling. J Immunol Methods 2009; 340: 55-64.
65. Contreras JP Ly NP Gold DR He H Wand M Weiss ST Perkins DL Platts-Mills TA Finn PW. Allergen-induced cytokine production, atopic disease, IgE, and wheeze in children. J Allergy Clin Immunol 2003; 112: 1072-7.
66. McQuaid EL Walders N Kopel SJ Fritz GK Klinnert MD. Pediatric asthma management in the family context: the Family Asthma Management System Scale. J Pediatr Psychol 2005; 30: 492-502.
67. Miller MR Hankinson J Brusasco V Burgos F Casaburi R Coates A Crapo R Enright P van der Grinten CP Gustafsson P Jensen R Johnson DC MacIntyre N McKay R Navajas D Pedersen OF Pellegrino R Viegi G Wanger J. ATS/ERS TF: standardisation of spirometry. Eur Respir J 2005; 26: 319-38.
68. Childhood Asthma Management Program Research Group: The Childhood Asthma Management Program (CAMP): design, rationale, and methods. Control Clin Trials 1999; 20: 91-120.
69. Wang XB Dockery DW Wypij D Fay ME Ferris BG. Pulmonary function between 6 and 18 years of age. Pediatr Pulmonol 1993; 15: 75-88.
70. Nathan RA Sorkness CA Kosinski M Schatz M Li JT Marcus P Murray JJ Pendergraft TB. Development of the asthma control test: a survey for assessing asthma control. J Allergy Clin Immunol 2004; 113: 59-65.
71. Schatz M Sorkness CA Li JT Marcus P Murray JJ Nathan RA Kosinski M Pendergraft TB Jhingran P. Asthma control test: reliability, validity, and responsiveness in patients not previously followed by asthma specialists. J Allergy Clin Immunol 2006; 117: 549-56.
72. Juniper EF Guyatt GH Feeny DH Ferrie PJ Griffith LE Townsend M. Measuring quality of life in children with asthma. Qual Life Res 1996; 5: 35-46.
73. Holtzman MJ Morton JD Shornick LP Tyner JW O'Sullivan MP Antao A Lo M Castro M Walter MJ. Immunity, inflammation, and remodeling in the airway epithelial barrier: epithelial-viral-allergic paradigm. Physiol Rev 2002; 82: 19-46.
74. Chen E Miller GE. Stress and inflammation in exacerbations of asthma. Brain Behav Immun 2007; 21: 993-9.
75. Wright RJ Cohen RT Cohen S. The impact of stress on the development and expression of atopy. Curr Opin Allergy Clin Immunol 2005; 5: 23-9.
76. Liu LY Coe CL Swenson CA Kelly EA Kita H Busse WW. School examinations enhance airway inflammation to antigen challenge. Am J Respir Crit Care Med 2002; 165: 1062-7.
77. Adler NE Snibbe AC. The role of psychosocial processes in explaining the gradient between socioeconomic status and health. Curr Dir Psychol Sci 2003; 12: 119-23.
78. Lantz PM House JS Lepkowski JM Williams DR Mero RP Chen J. Socioeconomic factors, health behaviors, and mortality: results from a nationally representative prospective study of US adults. JAMA 1998; 279: 1703-8.