Sleep disturbances increase interleukin-6 production during pregnancy: Implications for pregnancy complications

Reproductive Sciences

Volumn 14, Issue 6, 2007, Pages 560-567

  Okun, Michele L ^a,b   Hall, Martica ^a   Coussons Read, Mary E ^b  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Cytokines; Interleukin 6; Pregnancy complications; Sleep

Indexed keywords

INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; IL6 PROTEIN, HUMAN; LIPOPOLYSACCHARIDE; LIPOPOLYSACCHARIDE, ESCHERICHIA COLI 0111 B4; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HUMAN; HUMAN CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PREGNANCY; PREGNANCY COMPLICATION; PRIORITY JOURNAL; QUESTIONNAIRE; SLEEP DISORDER; BLOOD; CELL CULTURE; CROSS-SECTIONAL STUDY; DRUG EFFECT; FIRST TRIMESTER PREGNANCY; INFLAMMATION; METABOLISM; MONONUCLEAR CELL; PATHOPHYSIOLOGY; SECOND TRIMESTER PREGNANCY; SLEEP; THIRD TRIMESTER PREGNANCY; UPREGULATION;

ADULT; CELLS, CULTURED; CROSS-SECTIONAL STUDIES; FEMALE; HUMANS; INFLAMMATION; INTERLEUKIN-6; LEUKOCYTES, MONONUCLEAR; LIPOPOLYSACCHARIDES; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANCY TRIMESTER, FIRST; PREGNANCY TRIMESTER, SECOND; PREGNANCY TRIMESTER, THIRD; QUESTIONNAIRES; SLEEP; SLEEP DISORDERS; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 38449086375     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719107307647     Document Type: Article

References (68)

1. Hertz G., Fast A., Feinsilver SH, Albertario CL, Schulman H., Fein AM Sleep in normal late pregnancy. Sleep. 1992 ; 15 (3). 246-251.
2. Lee KA, Zaffke ME, McEnany G. Parity and sleep patterns during and after pregnancy. Obstet Gynecol. 2000 ; 95 (1). 14-18.
3. Mindell JA, Jacobson BJ Sleep disturbances during pregnancy. J Obstet Gynecol Neonatal Nurs. 2000 ; 29 (6). 590-597.
4. Okun ML, Coussons-Read ME Sleep disruption during pregnancy: how does it influence serum cytokines? J Reprod Immunol. 2007 ; 73 (2). 158-165.
5. Breslau N., Roth T., Rosenthal L., Andreski P. Sleep disturbance and psychiatric disorders: a longitudinal epidemiological study of young adults. Biol Psychiatry. 1996 ; 39 (6). 411-418.
6. Ford DE, Cooper-Patrick L. Sleep disturbances and mood disorders: an epidemiologic perspective. Depress Anxiety. 2001 ; 14 (1). 3-6.
7. Perlis ML, Giles DE, Buysse DJ, Tu X., Kupfer DJ Self-reported sleep disturbance as a prodromal symptom in recurrent depression. J Affect Disord. 1997 ; 42 (2-3). 209-212.
8. Jennings JR, Muldoon MF, Hall M., Buysse DJ, Manuck SB Self-reported sleep quality is associated with the metabolic syndrome. Sleep. 2007 ; 30 (2). 219-223.
9. Knutson KL, Ryden AM, Mander BA, Van Cauter E. Role of sleep duration and quality in the risk and severity of type 2 diabetes mellitus. Arch Intern Med. 2006 ; 166 (16). 1768-1774.
10. Meisinger C., Heier M., Loewel H. Sleep disturbance as a predictor of type 2 diabetes mellitus in men and women from the general population. Diabetologia. 2005 ; 48 (2). 235-241.
11. Punjabi NM, Ahmed MM, Polotsky VY, Beamer BA, O'Donnell CP Sleep-disordered breathing, glucose intolerance, and insulin resistance. Respir Physiol Neurobiol. 2003 ; 136 (2-3). 167-178.
12. Spiegel K., Knutson K., Leproult R., Tasali E., Van Cauter E. Sleep loss: a novel risk factor for insulin resistance and type 2 diabetes. J Appl Physiol. 2005 ; 99 (5). 2008-2019.
13. Vgontzas AN, Papanicolaou DA, Bixler EO, et al. Sleep apnea and daytime sleepiness and fatigue: relation to visceral obesity, insulin resistance, and hypercytokinemia. J Clin Endocrinol Metab. 2000 ; 85 (3). 1151-1158.
14. Dimitrov S., Lange T., Tieken S., Fehm HL, Born J. Sleep associated regulation of T helper 1/T helper 2 cytokine balance in humans. Brain Behav Immun. 2004 ; 18 (4). 341-348.
15. Irwin MR, Wang M., Campomayor CO, Collado-Hidalgo A., Cole S. Sleep deprivation and activation of morning levels of cellular and genomic markers of inflammation. Arch Intern Med. 2006 ; 166 (16). 1756-1762.
16. Redwine L., Hauger RL, Gillin JC, Irwin M. Effects of sleep and sleep deprivation on interleukin-6, growth hormone, cortisol, and melatonin levels in humans. J Clin Endocrinol Metab. 2000 ; 85 (10). 3597-3603.
17. von Kanel R., Dimsdale JE, Ancoli-Israel S., et al. Poor sleep is associated with higher plasma proinflammatory cytokine interleukin-6 and procoagulant marker fibrin D-dimer in older caregivers of people with Alzheimer's disease. J Am Geriatr Soc. 2006 ; 54 (3). 431-437.
18. Vgontzas AN, Papanicolaou DA, Bixler EO, et al. Circadian interleukin-6 secretion and quantity and depth of sleep. J Clin Endocrinol Metab. 1999 ; 84 (8). 2603-2607.
19. Himmerich H., Beitinger PA, Fulda S., et al. Plasma levels of tumor necrosis factor alpha and soluble tumor necrosis factor receptors in patients with narcolepsy. Arch Intern Med. 2006 ; 166 (16). 1739-1743.
20. Vgontzas AN, Zoumakis E., Bixler EO, et al. Adverse effects of modest sleep restriction on sleepiness, performance, and inflammatory cytokines. J Clin Endocrinol Metab. 2004 ; 89 (5). 2119-2126.
21. Qiu C., Sorensen TK, Luthy DA, Williams MA A prospective study of maternal serum C-reactive protein (CRP) concentrations and risk of gestational diabetes mellitus. Paediatr Perinat Epidemiol. 2004 ; 18 (5). 377-384.
22. Romero R., Espinoza J., Goncalves LF, Kusanovic JP, Friel LA, Nien JK Inflammation in preterm and term labour and delivery. Semin Fetal Neonatal Med. 2006 ; 11 (5). 317-326.
23. Dinarello CA Proinflammatory cytokines. Chest. 2000 ; 118 (2). 503-508.
24. Afshari JT, Ghomian N., Shameli A., et al. Determination of interleukin-6 and tumor necrosis factor-alpha concentrations in Iranian-Khorasanian patients with preeclampsia. BMC Pregnancy Childbirth. 2005 ; 5: 14.
25. Ategbo JM, Grissa O., Yessoufou A., et al. Modulation of adipokines and cytokines in gestational diabetes and macrosomia. J Clin Endocrinol Metab. 2006 ; 91 (10). 4137-4143.
26. Bartha JL, Romero-Carmona R., Comino-Delgado R. Inflammatory cytokines in intrauterine growth retardation. Acta Obstet Gynecol Scand. 2003 ; 82 (12). 1099-1102.
27. Backhaus J., Jughanns K., Broocks A., Riemann D., Hohagen F. Test-retest reliability and validity of the Pittsburgh Sleep Quality Index in primary insomnia. J Psychosom Res. 2002 ; 53 (3). 737-740.
28. Buysse DJ, Reynolds CF, Monk TH, Berman SR, Kupfer DJ The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989 ; 28: 193-213.
29. Carpenter JS, Andrykowski MA Psychometric evaluation of the Pittsburgh Sleep Quality Index. J Psychosom Res. 1998 ; 45 (1 Spec No). 5-13.
30. Quan SF, Howard BV, Iber C., et al. The Sleep Heart Health Study: design, rationale, and methods. Sleep. 1997 ; 20 (12). 1077-1085.
31. Tishler PV, Larkin EK, Schluchter MD, Redline S. Incidence of sleep-disordered breathing in an urban adult population: the relative importance of risk factors in the development of sleep-disordered breathing. JAMA. 2003 ; 289 (17). 2230-2237.
32. Young T., Peppard PE, Gottlieb DJ Epidemiology of obstructive sleep apnea: a population health perspective. Am J Respir Crit Care Med. 2002 ; 165 (9). 1217-1239.
33. Walsleben JA, Kapur VK, Newman AB, et al. Sleep and reported daytime sleepiness in normal subjects: the Sleep Heart Health Study. Sleep. 2004 ; 27 (2). 293-298.
34. Lichstein KL, Durrence HH, Taylor DJ, Bush AJ, Riefel BW Quantitative criteria for insomnia. Behav Res Ther. 2003 ; 41 (4). 427-445.
35. Pien GW, Schwab RJ Sleep disorders during pregnancy. Sleep. 2004 ; 27 (7). 1405-1417.
36. Redwine L., Dang J., Hall M., Irwin M. Disordered sleep, nocturnal cytokines, and immunity in alcoholics. Psychosom Med. 2003 ; 65 (1). 75-85.
37. Vgontzas AN, Bixler EO, Lin HM, Prolo P., Trakada G., Chrousos GP IL-6 and its circadian secretion in humans. Neuroimmunomodulation. 2005 ; 12 (3). 131-140.
38. Hogan D., Morrow JD, Smith EM, Opp MR Interleukin-6 alters sleep of rats. J Neuroimmunol. 2003 ; 137 (1-2). 59-66.
39. Krueger JM, Fang J., Taishi P., Chen Z., Kushikata T., Gardi J. Sleep: a physiologic role for IL-1 beta and TNF-alpha. Ann N Y Acad Sci. 1998 ; 856: 148-159.
40. Everson CA Clinical assessment of blood leukocytes, serum cytokines, and serum immunoglobulins as responses to sleep deprivation in laboratory rats. Am J Physiol Reg Integr Comp Physiol. 2005 ; 289 (4). R1054 - R1063.
41. Opp M., Born J., Irwin M. Sleep and the immune system. In: Ader R, ed. Psychoneuroimmunology. 4 th ed. New York: Academic Press ; 2006: 539-578.
42. Okun ML, Giese S., Lin L., Einen M., Mignot E., Coussons-Read ME Exploring the cytokine and endocrine involvement in narcolepsy. Brain Behav Immun. 2004 ; 18 (4). 326-332.
43. Vgontzas AN, Papanicolaou DA, Bixler EO, Kales A., Tyson K., Chrousos GP Elevation of plasma cytokines in disorders of excessive daytime sleepiness: role of sleep disturbance and obesity. J Clin Endocrinol Metab. 1997 ; 82 (5). 1313-1316.
44. Friedman EM, Hayney MS, Love GD, et al. Social relationships, sleep quality, and interleukin-6 in aging women. Proc Natl Acad Sci U S A. 2005 ; 102 (51). 18757-18762.
45. Salas-Salvado J., Bullo M., Garcia-Lorda P., et al. Subcutaneous adipose tissue cytokine production is not responsible for the restoration of systemic inflammation markers during weight loss. Int J Obes (Lond). 2006 ; 30 (12). 1714-1720.
46. Stotland NE, Haas JS, Brawarsky P., Jackson RA, Fuentes-Afflick E., Escobar GJ Body mass index, provider advice, and target gestational weight gain. Obstet Gynecol. 2005 ; 105 (3). 633-638.
47. Ciftci TU, Kokturk O., Bukan N., Bilgihan A. The relationship between serum cytokine levels with obesity and obstructive sleep apnea syndrome. Cytokine. 2004 ; 28 (2). 87-91.
48. Arntzen KJ, Kjollesdal AM, Halgunset J., Vatten L., Austgulen R. TNF, IL-1, IL-6, IL-8 and soluble TNF receptors in relation to chorioamnionitis and premature labor. J Perinat Med. 1998 ; 26 (1). 17-26.
49. Azizieh F., Raghupathy R., Makhseed M. Maternal cytokine production patterns in women with pre-eclampsia. Am J Reprod Immunol. 2005 ; 54 (1). 30-37.
50. Edwards N., Blyton CM, Kesby GJ, Wilcox I., Sullivan CE Pre-eclampsia is associated with marked alterations in sleep architecture. Sleep. 2000 ; 23 (5). 619-625.
51. Ekholm EM, Polo O., Rauhala ER, Ekblad UU Sleep quality in preeclampsia. Am J Obstet Gynecol. 1992 ; 167 (5). 1262-1266.
52. Lee KA, Gay CL Sleep in late pregnancy predicts length of labor and type of delivery. Am J Obstet Gynecol. 2004 ; 191 (6). 2041-2046.
53. Kimura M., Zhang SQ, Inoue S. Pregnancy-associated sleep changes in the rat. Am J Physiol. 1996 ; 271 (4 pt 2). R1063 - R1069.
54. Krueger JM, Obal F. Jr, Fang J., Kubota T., Taishi P. The role of cytokines in physiological sleep regulation. Ann N Y Acad Sci. 2001 ; 933 (1). 211-221.
55. Opp MR Cytokines and sleep. Sleep Med Rev. 2005 ; 9 (5). 355-364.
56. Frey DJ, Fleshner M., Wright KP Jr. The effects of 40 hours of total sleep deprivation on inflammatory markers in healthy young adults. Brain Behav Immun. Epub ahead of print May 22, 2007.
57. Irwin M. Effects of sleep and sleep loss on immunity and cytokines. Brain Behav Immun. 2002 ; 16 (5). 503-512.
58. Irwin M., McClintick J., Costlow C., Fortner M., White J., Gillin JC Partial night sleep deprivation reduces natural killer and cellular immune responses in humans. FASEB J. 1996 ; 10 (5). 643-653.
59. Shearer WT, Reuben JM, Mullington JM, et al. Soluble TNF-alpha receptor 1 and IL-6 plasma levels in humans subjected to the sleep deprivation model of spaceflight. J Allergy Clin Immunol. 2001 ; 107 (1). 165-170.
60. Conrad KP, Miles TM, Benyo DF Circulating levels of immunoreactive cytokines in women with preeclampsia. Am J Reprod Immunol. 1998 ; 40 (2). 102-111.
61. Luppi P., DeLoia JA Monocytes of preeclamptic women spontaneously synthesize pro-inflammatory cytokines. Clin Immunol. 2006 ; 118 (2-3). 268-275.
62. Munno I., Chiechi LM, Lacedra G., et al. Spontaneous and induced release of prostaglandins, interleukin (IL)-1beta, IL-6, and tumor necrosis factor-alpha by placental tissue from normal and preeclamptic pregnancies. Am J Reprod Immunol. 1999 ; 42 (6). 369-374.
63. Meier-Ewert HK, Ridker PM, Rifai N., Price N., Dinges DF, Mullington JM Absence of diurnal variation of C-reactive protein concentrations in healthy human subjects. Clin Chem. 2001 ; 47 (3). 426-430.
64. Maasilta P., Bachour A., Teramo K., Polo O., Laitinen LA Sleep-related disordered breathing during pregnancy in obese women. Chest. 2001 ; 120 (5). 1448-1454.
65. Guilleminault C., Kirisoglu C., Ohayon MM C-reactive protein and sleep-disordered breathing. Sleep. 2004 ; 27 (8). 1507-1511.
66. Yao M., Tachibana N., Okura M., et al. The relationship between sleep-disordered breathing and high-sensitivity C-reactive protein in Japanese men. Sleep. 2006 ; 29 (5). 661-665.
67. Yinon D., Lowenstein L., Suraya S., et al. Pre-eclampsia is associated with sleep-disordered breathing and endothelial dysfunction. Eur Respir J. 2006 ; 27 (2). 328-333.
68. Roberts JM Pregnancy-related hypertension. In: Creasey RK, Resnik R, eds. Maternal-Fetal Medicine. Philadelphia, PA: Saunders ; 2004: 859-899.