Inflammation, Reproduction, and the Goldilocks Principle

Part of the Developments in Primatology: Progress and Prospects book series (DIPR, volume 37)


Modulation of reproductive function in response to ecological stressors allows an individual to conceive and carry a fetus under optimal conditions relative to that individual’s environment. Stress can affect inflammation and inflammatory processes that are integral to reproductive function. Ovulation and implantation, in particular, are driven by local expression of cytokines in the granulosa cells and endometrial tissue, and some evidence suggests that local expression may be impacted by ecological factors impacting systemic inflammation. Further, ovarian hormones are often mediators of inflammatory processes that control endometrial functioning, and tissue remodeling that occurs in both the proliferative and secretory phases of the endometrial cycle is also inflammatory in nature.As a result, the study of ovarian and endometrial functioning creates the opportunity to test questions regarding a trade-off that characterizes human pregnancy: close maternal-fetal contact to improve resource transmission, yet higher vulnerabilities to pathologies related to energetics and inflammation such as gestational diabetes and choriodecidual inflammatory syndrome. Several ecological factors have been shown to impact reproductive functioning: psychosocial stress, energetics, and immunological stress. While those with the strongest correlative effect are energetic, both psychosocial and immunological stresses are relevant to this discussion because the stress response – particularly when chronically activated – induces inflammation. Previous and new research both on psychosocial stressors and inflammatory processes have found tenuous relationships with reproductive hormones and menstrual cycle length. Further, inflammation has a significant impact on fetal loss Thus, the goal of this chapter is to demonstrate what evidence supports a relationship between inflammation and reproductive functioning, how ecological factors that induce inflammation produces variation in rates of ovulation, implantation, and fetal loss, and how such relationships might be better tested in future work.


Inflammation C-reactive protein Ovarian function Endometrial function Pregnancy Reproductive ecology Human 


  1. Agic A, Xu H, Finas D, Banz C, Diedrich K, Hornung D (2006) Is endometriosis associated with systemic subclinical inflammation? Gynecol Obstet Invest 62:139–147PubMedGoogle Scholar
  2. Aiello AE, Diez-Roux A, Noone AM, Ranjit N, Cushman M, Tsai MY, Szklo M (2009) Socioeconomic and psychosocial gradients in cardiovascular pathogen burden and immune response: the multi-ethnic study of atherosclerosis. Brain Behav Immun 23:663–671PubMedGoogle Scholar
  3. Allsworth J, Clarke J, Peipert J, Hebert M, Cooper A, Boardman L (2007) The influence of stress on the menstrual cycle among newly incarcerated women. Womens Health Issues 17:202–209PubMedGoogle Scholar
  4. Almagor M, Hazav A, Yaffe H (2004) The levels of C-reactive protein in women treated by IVF. Hum Reprod 19:104–106PubMedGoogle Scholar
  5. Anumba D, El Gelany S, Elliott S, Li T (2010) Circulating levels of matrix proteases and their inhibitors in pregnant women with and without a history of recurrent pregnancy loss. Reprod Biol Endocrinol 8:62PubMedGoogle Scholar
  6. Baerwald A, Adams G, Pierson R (2003a) Characteristics of ovarian follicular wave dynamics in women. Biol Reprod 69:1023–1031PubMedGoogle Scholar
  7. Baerwald A, Adams G, Pierson R (2003b) A new model for ovarian follicular development during the human menstrual cycle. Fertil Steril 80:116–122PubMedGoogle Scholar
  8. Baird D (1987) A model for follicular selection and ovulation: lessons from superovulation. J Steroid Biochem 27:15–23PubMedGoogle Scholar
  9. Bakos O, Lundkvist O, Wide L, Bergh T (1994) Ultrasonographical and hormonal description of the normal ovulatory menstrual cycle. Acta Obstet Gynecol Scand 73:790–796PubMedGoogle Scholar
  10. Barnes K, Armelagos G, Morreale S (1999) Darwinian medicine and the emergence of allergy. In: Trevathan W, Smith E, McKenna J (eds) Evolutionary medicine. Oxford University Press, New YorkGoogle Scholar
  11. Barrett R, Harlan L, Wesley M, Hill H, Chen V, Clayton L, Kotz H, Eley J, Robboy S, Edwards B (1995) Endometrial cancer: stage at diagnosis and associated factors in black and white patients. Am J Obstet Gynecol 173:414–422PubMedGoogle Scholar
  12. Basar M, Yen C-F, Buchwalder LF, Murk W, Huang SJ, Godlewski K, Kocamaz E, Arda O, Schatz F, Lockwood CJ, Kayisli UA (2010) Preeclampsia-related increase of interleukin-11 expression in human decidual cells. Reproduction 140:605–612PubMedGoogle Scholar
  13. Baynard T, Carhart JR, Ploutz-Snyder L, Weinstock R, Kanaley J (2008) Short-term training effects on diastolic function in obese individuals, with and without the metabolic syndrome. Obesity 16:1277–1283PubMedGoogle Scholar
  14. Bedaiwy M, Shahin A, AbulHassan A, Goldberg J, Sharma R, Agarwal A, Falcone T (2007) Differential expression of follicular fluid cytokines: relationship to subsequent pregnancy in IVF cycles. Reprod Biomed Online 15:321–325PubMedGoogle Scholar
  15. Beier H, Beier-Hellwig K (1998) Molecular and cellular aspects of endometrial receptivity. Hum Reprod Update 4:448–458PubMedGoogle Scholar
  16. Belalcazar LM, Reboussin DM, Haffner SM, Hoogeveen RC, Kriska AM, Schwenke DC, Tracy RP, Pi-Sunyer FX, Ballantyne CM, Group ftLAR (2010) A 1-year lifestyle intervention for weight loss in individuals with type 2 diabetes reduces high C-reactive protein levels and identifies metabolic predictors of change. Diabetes Care 33:2297–2303PubMedGoogle Scholar
  17. Bischof P, Meisser A, Campana A (1998) Involvement of trophoblast in embryo implantation: regulation by paracrine factors. J Reprod Immunol 39:167–177PubMedGoogle Scholar
  18. Block E (1951) Quantitative morphological investigations of the follicular system in women: variations in the different phases of the sexual cycle. Acta Endocrinol 8:33–54PubMedGoogle Scholar
  19. Boggess K, Lieff S, Murtha A, Moss K, Jared H, Beck J, Offenbacher S (2005) Maternal serum C-reactive protein concentration early in pregnancy and subsequent pregnancy loss. Am J Perinatol 22:299–304PubMedGoogle Scholar
  20. Borders A, Grobman W, Amsden L, Holl J (2007) Chronic stress and low birth weight neonates in a low-income population of women. Obstet Gynecol 109:331–338PubMedGoogle Scholar
  21. Borders AEB, Grobman WA, Amsden LB, McDade TW, Sharp LK, Holl JL (2010) The relationship between self-report and biomarkers of stress in low-income reproductive-age women. Am J Obstet Gynecol 203:577. e1–577. e8Google Scholar
  22. Bribiescas RG (2005) Serum leptin levels in Ache Amerindian females with normal adiposity are not significantly different from American anorexia nervosa patients. Am J Hum Biol 17:207–210PubMedGoogle Scholar
  23. Brinton LA, Lamb EJ, Moghissi KS, Scoccia B, Althuis MD, Mabie JE, Westhoff CL (2004) Ovarian cancer risk associated with varying causes of infertility. Fertil Steril 82:405–414PubMedGoogle Scholar
  24. Chenillot O, Henny J, Steinmetz J, Herbeth B, Wagner C, Siest G (2000) High sensitivity C-reactive protein: biological variations and reference limits. Clin Chem Lab Med 38:1003–1011PubMedGoogle Scholar
  25. Chisholm JS, Quinlivan JA, Petersen RW, Coall DA (2005) Early stress predicts age at menarche and first birth, adult attachment, and expected lifespan. Hum Nat 16:233–265Google Scholar
  26. Chrysohoou C, Panagiotakos DB, Pitsavos C, Das UN, Stefanadis C (2004) Adherence to the Mediterranean diet attenuates inflammation and coagulation process in healthy adults: the Attica study. J Am Coll Cardiol 44:152–158PubMedGoogle Scholar
  27. Clancy K, Tribble K, Klein L (2011) Pro- and anti-inflammatory food proteins and their impact on maternal ecology (abstract). Am J Phys Anthropol 144:109Google Scholar
  28. Clancy K, Klein L, Ziomkiewicz A, Nenko I, Jasienska G, Bribiescas R (2012) C-reactive protein is negatively correlated with reproductive hormones in a rural Polish population: implications for pooled energy budgets (in preparation)Google Scholar
  29. Clancy KBH, Ahern DT, Klein LD (2012) The relationship between strenuous physical activity and C-reactive protein is cycle-phase dependent: results from rural Poland (abstract). Am J Phys Anthropol 147:116Google Scholar
  30. Clancy KBH, Baerwald AR, Pierson RA (2012) C-reactive protein (CRP) in relation to follicle wave dynamics during the spontaneous menstrual cycle. PLoS One (under review)Google Scholar
  31. Coussons-Read ME Okun ML, Nettles CD (2007) Psychosocial stress increases inflammatory markers and alters cytokine production across pregnancy. Brain, Behavior and Immunity. 21:343–350PubMedGoogle Scholar
  32. Crespi B, Semeniuk C (2004) Parent-offspring conflict in the evolution of vertebrate reproductive mode. Am Nat 163:635–653PubMedGoogle Scholar
  33. Cunnane G (2001) Amyloid precursors and amyloidosis in inflammatory arthritis. Curr Opin Rheumatol 13:67PubMedGoogle Scholar
  34. Danese A, Moffitt TE, Harrington H, Milne BJ, Polanczyk G, Pariante CM, Poulton R, Caspi A (2009) Adverse childhood experiences and adult risk factors for age-related disease: depression, inflammation, and clustering of metabolic risk markers. Arch Pediatr Adolesc Med 163:1135–1143PubMedGoogle Scholar
  35. De Silva D, Mitchell M, Keelan J (2010) Inhibition of choriodecidual cytokine production and inflammatory gene expression by selective I-kappaB kinase (IKK) inhibitors. Br J Pharmacol 160:1808–1822PubMedGoogle Scholar
  36. Demir AY, Groothuis PG, Dunselman GAJ, Schurgers L, Evers JLH, de Goeij AFPM (2005) Molecular characterization of soluble factors from human menstrual effluent that induce epithelial to mesenchymal transitions in mesothelial cells. Cell Tissue Res 322:299–311PubMedGoogle Scholar
  37. Demir B, Guven S, Guven E, Atamer Y, Gul T (2009) Serum IL-6 level may have role in the pathophysiology of unexplained infertility. Am J Reprod Immunol 62:261–267PubMedGoogle Scholar
  38. Dervain I (1980) Etude echographique de la croissance du follice ovarian normal et detection de l’ovulation. Strasbourg (see:
  39. Dokras A, Baredziak L, Blaine J, Syrop C, VanVoorhis BJ, Sparks A (2006) Obstetric outcomes after in vitro fertilization in obese and morbidly obese women. Obstet Gynecol 108:61PubMedGoogle Scholar
  40. Dole N, Savitz D, Hertz-Picciotto I, Siega-Riz A, McMahon M, Buekens P (2003) Maternal stress and preterm birth. Am J Epidemiol 157:14–24PubMedGoogle Scholar
  41. Donofrio G, Capocefalo A, Franceschi V, Price S, Cavirani S, Sheldon M (2010) The Chemokine IL8 is up-regulated in bovine endometrial stromal cells by the BoHV-4 IE2 gene product, ORF50/Rta: a step ahead toward a mechanism for BoHV-4 induced endometritis. Biol Reprod 6;86:919–928Google Scholar
  42. Ellis BJ, Garber J (2000) Psychosocial antecedents of variation in girls’ pubertal timing: maternal depression, stepfather presence, and marital and family stress. Child Dev 71:485–501PubMedGoogle Scholar
  43. Ellison P, Lipson S, Jasienska G, Ellison P (2007) Moderate anxiety, whether acute or chronic, is not associated with ovarian suppression in healthy, well-nourished, western women. Am J Phys Anthropol 134:513–519PubMedGoogle Scholar
  44. Fehring RJ, Schneider M, Raviele K (2006) Variability in the phases of the menstrual cycle. J Obstet Gynecol Neonatal Nurs 35:376–384. doi: 10.1111/j.1552-6909.2006.00051.x PubMedGoogle Scholar
  45. Ficicioglu C, Kumbak B, Akcin O, Attar R, Yildirim G, Yesildaglar N (2010) Comparison of follicular fluid and serum cytokine concentrations in women undergoing assisted reproductive treatment with GnRH agonist long and antagonist protocols. Gynecol Endocrinol 26:181–186PubMedGoogle Scholar
  46. Finn C (1998) Menstruation: a nonadaptive consequence of uterine evolution. Q Rev Biol 73:163–173PubMedGoogle Scholar
  47. Flinn MV, England BG (2003) Childhood stress: endocrine and immune responses to psychosocial events. In Social & cultural lives of immune systems Wilce J.M (ed). pp. 107–147. London, UK:Routledge Press.Google Scholar
  48. Flores E, Tschann JM, Dimas JM, Bachen EA, Pasch LA, de Groat CL (2008) Perceived discrimination, perceived stress, and mental and physical health among Mexican-origin adults. Hispanic J Behav Sci 30:401–424Google Scholar
  49. Forsythe LK, Wallace J, Livingstone M (2008) Obesity and inflammation: the effects of weight loss. Nutr Res Rev 21:117–133PubMedGoogle Scholar
  50. Furuichi T, Gi I, Ihobe H, Kuroda S, Kitamura K, Mori A, Enomoto T, Okayasu N, Hashimoto C, Kano T (1998) Population dynamics of wild Bonobos (Pan paniscus) at Wamba. Int J Primatol 19:1029–1043Google Scholar
  51. Galdikas BMF, Wood JW (1990) Birth spacing patterns in humans and apes. Am J Phys Anthropol 83:185–191PubMedGoogle Scholar
  52. Gnainsky Y, Granot I, Aldo PB, Barash A, Or Y, et al. (2010) Local injury of the endometrium induces an inflammatory response that promotes successful implantation. Fertil Steril 94:2030–2036Google Scholar
  53. Gougeon A (1979) Qualitative changes in medium and large antral follicles in the human ovary during the menstrual cycle. Annals Biol Anim Bioch Biophys 19:1464–1468Google Scholar
  54. Gull B, Karlsson B, Milsom I, Granberg S (2001) Factors associated with endometrial thickness and uterine size in a random sample of postmenopausal women. Am J Obstet Gynecol 185:386–391PubMedGoogle Scholar
  55. Gurven M, Kaplan H, Winking J, Rodriguez DE, Vasunilashorn S, Kim JK, Finch C, Crimmins E (2009) Inflammation and infection do not promote arterial aging and cardiovascular disease risk factors among lean horticulturalists. PLoS One 4:376–398Google Scholar
  56. Guthrie BJ, Young AM, Williams DR, Boyd CJ, Kintner EK (2002) African American girls’ smoking habits and day-to-day experiences with racial discrimination. Nurs Res 51:183PubMedGoogle Scholar
  57. Guzelmeric K, Alkan N, Pirimoglu M, Unal O, Turan C (2007) Chronic inflammation and elevated homocysteine levels are associated with increased body mass index in women with polycystic ovary syndrome. Gynecol Endocrinol 23:505–510PubMedGoogle Scholar
  58. Hackeloer BJ, Fleming R, Robinson HP, Adam AH, Coutts JRT (1979) Correlation of ultrasonic and endocrinologic assessment of human follicular development. Am J Obstet Gynecol 135:122–128PubMedGoogle Scholar
  59. Haig D (1993) Genetic conflicts in human pregnancy. Q Rev Biol 68:495–532PubMedGoogle Scholar
  60. Hammadeh M, Ertan A, Georg M, Rosenbaum P, Schmidt W (2002) Relationship between ovarian stimulation regimen and interleukin level in pre-ovulatory follicular fluid and their effect on ICSI outcome. Am J Reprod Immunol 48:255–261PubMedGoogle Scholar
  61. Hauguel-de Mouzon S, Guerre-Millo M (2006) The placenta cytokine network and inflammatory signals. Placenta 27:794–798PubMedGoogle Scholar
  62. Heilbronn L, Noakes M, Clifton PM (2001) Energy restriction and weight loss on very-low-fat diets reduce C-reactive protein concentrations in obese, healthy women. Arterioscler Thromb Vasc Biol 21:968–970PubMedGoogle Scholar
  63. Hogue C, Hoffman S, Hatch M (2001) Stress and preterm delivery: a conceptual framework. Paediatr Perinat Epidemiol 15:30–40PubMedGoogle Scholar
  64. Honda H, Qureshi AR, Heimbürger O, Barany P, Wang K, Pecoits-Filho R, Stenvinkel P, Lindholm B (2006) Serum albumin, C-reactive protein, interleukin 6, and fetuin A as predictors of malnutrition, cardiovascular disease, and mortality in patients with ESRD. Am J Kidney Dis 47:139–148PubMedGoogle Scholar
  65. Hoshiai KOH (2000) Common genetic changes between endometriosis and ovarian cancer. Gynecol Obstet Invest 50:39–43PubMedGoogle Scholar
  66. Hutchinson WL, Koenig W, Frohlich M, Sund M, Lowe GDO, Pepys MB (2000) Immunoradiometric assay of circulating C-reactive protein: age-related values in the adult general population. Clin Chem 46:934–938PubMedGoogle Scholar
  67. Hvilsom GB, Thorsen P, Jeune B, Bakketeig LS (2002) C-reactive protein: a serological marker for preterm delivery? Acta Obstet Gynecol Scand 81:424–429PubMedGoogle Scholar
  68. Jasienska G, Ellison PT (1998) Physical work causes suppression of ovarian function in women. Proc R Soc Lond B 265:1847–1851Google Scholar
  69. Jilma B, Dirnberger E, Löscher I, Rumplmayr A, Hildebrandt J, Eichler H, Kapiotis S, Wagner O (1997) Menstrual cycle-associated changes in blood levels of interleukin-6, alpha1 acid glycoprotein, and C-reactive protein. J Lab Clin Med 130:69PubMedGoogle Scholar
  70. Kaaks R, Lukanova A, Kurzer MS (2002) Obesity, endogenous hormones, and endometrial cancer risk: a synthetic review. Cancer Epidemiol Biomarkers Prev 11:1531–1543PubMedGoogle Scholar
  71. Kaplan H (1996) A theory of fertility and parental investment in traditional and modern human societies. Yearbook of physical anthropology 39:91–136Google Scholar
  72. Kaplan HS, Lancaster JB (2003) An evolutionary and ecological analysis of human fertility, mating patterns, and parental investment. In: Wachter K, Bulatao R (eds) Offspring: human fertility behavior in biodemographic perspective. The National Academies Press, Washington, pp 170–223Google Scholar
  73. Kasapis C, Thompson PD (2005) The effects of physical activity on serum C-reactive protein and inflammatory markers: a systematic review. J Am Coll Cardiol 45:1563–1569PubMedGoogle Scholar
  74. Kasim-Karakas SE, Tsodikov A, Singh U, Jialal I (2006) Responses of inflammatory markers to a low-fat, high-carbohydrate diet: effects of energy intake. Am J Clin Nutr 83:774PubMedGoogle Scholar
  75. Kiecolt-Glaser JK, Gouin JP, Weng N, Malarkey WB, Beversdorf DQ, Glaser R (2011) Childhood adversity heightens the impact of later-life caregiving stress on telomere length and inflammation. Psychosom Med 73:16–22PubMedGoogle Scholar
  76. King AE, Critchley HO (2010) Oestrogen and progesterone regulation of inflammatory processes in the human endometrium. J Steroid Biochem Mol Biol 120:116–126Google Scholar
  77. King DE, Egan BM, Geesey ME (2003) Relation of dietary fat and fiber to elevation of C-reactive protein. Am J Cardiol 92:1335–1339PubMedGoogle Scholar
  78. Knoeller S, Lim E, Aleta L, Hertwig K, Dudenhausen J, Arck P (2003) Distribution of immunocompetent cells in decidua of controlled and uncontrolled (choriocarcinoma/hydatidiform mole) trophoblast invasion. Am J Reprod Immunol 50:41–47PubMedGoogle Scholar
  79. Knott C (2001) Female reproductive ecology of the apes: Implications for human evolution. In: Ellison P, editor. Reproductive Ecology and Human Evolution. New York: Aldine de Gruyter. pp. 429–463Google Scholar
  80. Koyanagi A, Kuffo D, Gresely L, Shenkin A, Cuevas L (2004) Relationships between serum concentrations of C-reactive protein and micronutrients, in patients with tuberculosis. Ann Trop Med Parasitol 98:391–399PubMedGoogle Scholar
  81. Lancaster JB, Kaplan HS, Hill K, Hurtado AM (2000) The evolution of life history, intelligence and diet among chimpanzees and human foragers. In: Tonneau F, Thompson N (eds) Perspectives in ethology. Kluwer Academic/Plenum, New York, pp 13–47Google Scholar
  82. LeBlanc M (2010) Advances in the diagnosis and treatment of chronic infectious and post-mating-induced endometritis in the mare. Reprod Domest Anim 45:21–27PubMedGoogle Scholar
  83. Lenz S (1985) Ultrasonic study of follicular maturation, ovulation and development of corpus luteum during normal menstrual cycles. Acta Obstet Gynecol Scand 64:15–19PubMedGoogle Scholar
  84. Lessey BA (2003) Two pathways of progesterone action in the human endometrium: implications for implantation and contraception. Steroids 68:809–815Google Scholar
  85. Levens ED, Skarulis MC (2008) Assessing the role of endometrial alteration among obese patients undergoing assisted reproduction. Fertil Steril 89:1606–1608PubMedGoogle Scholar
  86. Lewis TT, Aiello AE, Leurgans S, Kelly J, Barnes LL (2010) Self-reported experiences of ­everyday discrimination are associated with elevated C-reactive protein levels in older African-American adults. Brain Behav Immun 24:438–443PubMedGoogle Scholar
  87. Lewis TT, Kravitz HM, Janssen I, Powell LH (2011) Self-reported experiences of discrimination and visceral fat in middle-aged African-American and Caucasian women. Am J Epidemiol 173:1223PubMedGoogle Scholar
  88. Lightfoot JT (2008) Sex hormones’ regulation of rodent physical activity: a review. Int J Biol Sci 4:126PubMedGoogle Scholar
  89. Lipson SF, Ellison PT (1996) Comparison of salivary steroid profiles in naturally occurring conception and non-conception cycles. Hum Reprod 11:2090–2096PubMedGoogle Scholar
  90. Liu S, Manson JAE, Buring JE, Stampfer MJ, Willett WC, Ridker PM (2002) Relation between a diet with a high glycemic load and plasma concentrations of high-sensitivity C-reactive protein in middle-aged women. Am J Clin Nutr 75:492PubMedGoogle Scholar
  91. Lopez-Garcia E, Schulze MB, Fung TT, Meigs JB, Rifai N, Manson JAE, Hu FB (2004) Major dietary patterns are related to plasma concentrations of markers of inflammation and endothelial dysfunction. Am J Clin Nutr 80:1029PubMedGoogle Scholar
  92. Maheshwari A, Stofberg L, Bhattacharya S (2007) Effect of overweight and obesity on assisted reproductive technology—a systematic review. Hum Reprod Update 13:433–444PubMedGoogle Scholar
  93. Malik S, Day K, Perrault I, Charnock-Jones DS, Smith SK (2006) Reduced levels of VEGF-A and MMP-2 and MMP-9 activity and increased TNF- in menstrual endometrium and effluent in women with menorrhagia. Hum Reprod 21:2158PubMedGoogle Scholar
  94. Maybin JA, Critchley HOD, Jabbour HN (2011) Inflammatory pathways in endometrial disorders. Mol Cell Endocrinol 335:42–51PubMedGoogle Scholar
  95. Mays VM, Cochran SD, Barnes NW (2007) Race, race-based discrimination, and health outcomes among African Americans. Annu Rev Psychol 58:201–225PubMedGoogle Scholar
  96. McDade T, Leonard W, Burhop J, Reyes García V, Vadez V, Huanca T, Godoy R (2005) Predictors of C reactive protein in Tsimane’ 2 to 15 year olds in lowland Bolivia. Am J Phys Anthropol 128:906–913PubMedGoogle Scholar
  97. McDade TW, Hawkley LC, Cacioppo JT (2006) Psychosocial and behavioral predictors of inflammation in middle-aged and older adults: the Chicago health, aging, and social relations study. Psychosom Med 68:376–381PubMedGoogle Scholar
  98. McDade TW, Williams S, Snodgrass JJ (2007) What a drop can do: dried blood spots as a minimally invasive method for integrating biomarkers into population-based research. Demography 44:899–925PubMedGoogle Scholar
  99. McDade TW, Rutherford JN, Adair L, Kuzawa C (2008) Adiposity and pathogen exposure predict C-reactive protein in Filipino women. J Nutr 138:2442–2447PubMedGoogle Scholar
  100. McDade TW, Rutherford JN, Adair L, Kuzawa C (2009) Population differences in associations between C-reactive protein concentration and adiposity: comparison of young adults in the Philippines and the United States. Am J Clin Nutr 89:1237–1245PubMedGoogle Scholar
  101. McDade TW, Rutherford J, Adair L, Kuzawa CW (2010) Early origins of inflammation: microbial exposures in infancy predict lower levels of C-reactive protein in adulthood. Proc R Soc B Biol Sci 277(1684):1129–1137Google Scholar
  102. Merlini G, Bellotti V (2003) Molecular mechanisms of amyloidosis. N Engl J Med 349:583–596PubMedGoogle Scholar
  103. Miller GE, Stetler CA, Carney RM, Freedland KE, Banks WA (2002) Clinical depression and inflammatory risk markers for coronary heart disease. Am J Cardiol 90:1279–1283PubMedGoogle Scholar
  104. Miller GE, Rohleder N, Stetler C, Kirschbaum C (2005) Clinical depression and regulation of the inflammatory response during acute stress. Psychosom Med 67:679–687PubMedGoogle Scholar
  105. Miura S, Khan KN, Kitajima M, Hiraki K, Moriyama S, Masuzaki H, Samejima T, Fujishita A, Ishimaru T (2006) Differential infiltration of macrophages and prostaglandin production by different uterine leiomyomas. Hum Reprod 21:2545PubMedGoogle Scholar
  106. Modugno F, Ness RB, Chen C, Weiss NS (2005) Inflammation and endometrial cancer: a hypothesis. Cancer Epidemiol Biomarkers Prev 14:2840PubMedGoogle Scholar
  107. Morin-Papunen L, Rautio K, Ruokonen A, Hedberg P, Puukka M, Tapanainen J (2003) Metformin reduces serum C-reactive protein levels in women with polycystic ovary syndrome. J Clin Endocrinol Metab 88:4649PubMedGoogle Scholar
  108. Mustapha IZ, Debrey S, Oladubu M, Ugarte R (2007) Markers of systemic bacterial exposure in periodontal disease and cardiovascular disease risk: a systematic review and meta-analysis. J Periodontol 78:2289–2302PubMedGoogle Scholar
  109. Nazmi A, Victora C (2007) Socioeconomic and racial/ethnic differentials of C-reactive protein levels: a systematic review of population-based studies. BMC Public Health 7:212PubMedGoogle Scholar
  110. Nepomnaschy PA, Welch K, McConnell D, Strassmann BI, England BG (2004) Stress and female reproductive function: a study of daily variations in cortisol, gonadotrophins, and gonadal steroids in a rural Mayan population. Am J Hum Biol 16:523–532PubMedGoogle Scholar
  111. Nepomnaschy P, Welch K, McConnell D, Low B, Strassmann B, England B (2006) Cortisol levels and very early pregnancy loss in humans. Proc Natl Acad Sci USA 103:3938–3942PubMedGoogle Scholar
  112. Ness RB, Cottreau C (1999) Possible role of ovarian epithelial inflammation in ovarian cancer. JNCI J Natl Canc Inst 91:1459Google Scholar
  113. Nicklas BJ, Ambrosius W, Messier SP, Miller GD, Penninx BWJH, Loeser RF, Palla S, Bleecker E, Pahor M (2004) Diet-induced weight loss, exercise, and chronic inflammation in older, obese adults: a randomized controlled clinical trial. Am J Clin Nutr 79:544PubMedGoogle Scholar
  114. Nicklas BJ, You T, Pahor M (2005) Behavioural treatments for chronic systemic inflammation: effects of dietary weight loss and exercise training. Can Med Assoc J 172:1199–1209Google Scholar
  115. Nishida M, Watanabe K, Sato N, Ichikawa Y (2000) Malignant transformation of ovarian endometriosis. Gynecol Obstet Invest 50:18–25PubMedGoogle Scholar
  116. Noakes M, Keogh JB, Foster PR, Clifton PM (2005) Effect of an energy-restricted, high-protein, low-fat diet relative to a conventional high-carbohydrate, low-fat diet on weight loss, body composition, nutritional status, and markers of cardiovascular health in obese women. Am J Clin Nutr 81:1298PubMedGoogle Scholar
  117. Noyes N, Hampton B, Berkeley A, Licciardi F, Grifo J, Krey L (2001) Factors useful in predicting the success of oocyte donation: a 3-year retrospective analysis. Fertil Steril 76:92–97PubMedGoogle Scholar
  118. O’Herlihy C (1980) Monitoring ovarian follicular development with real-time ultrasound. Br J Obstet Gynaecol 87:613–618PubMedGoogle Scholar
  119. Oh J, Lee J-A, Lee H, Oh J-Y, Sung Y-A, Chung H (2009) Serum C-reactive protein levels in normal-weight polycystic ovary syndrome. Korean J Intern Med 24:350–355PubMedGoogle Scholar
  120. Orvieto R, Chen R, Ashkenazi J, Ben-Harush A, Bar J, Fisch B (2004) C-reactive protein levels in patients undergoing controlled ovarian hyperstimulation for IVF cycle. Hum Reprod 19:357–359PubMedGoogle Scholar
  121. Pache T, Wladimiroff J, DeJong F, Hop W, Fauser B (1990) Growth patterns of nondominant ovarian follicles during the normal menstrual cycle. Fertil Steril 54:638–642PubMedGoogle Scholar
  122. Pascoe EA, Smart RL (2009) Perceived discrimination and health: a meta-analytic review. Psychol Bull 135:531PubMedGoogle Scholar
  123. Paul K, Boutain D, Agnew K, Thomas J, Hitti J (2008) The relationship between racial identity, income, stress and C-reactive protein among parous women: implications for preterm birth disparity research. J Natl Med Assoc 100:540–546PubMedGoogle Scholar
  124. Picklesimer AH, Jared HL, Moss K, Offenbacher S, Beck JD, Boggess KA (2008) Racial differences in C-reactive protein levels during normal pregnancy. Am J Obstet Gynecol 199(523):e1–e6PubMedGoogle Scholar
  125. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM (2001) C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 286:327–334PubMedGoogle Scholar
  126. Queenan JT, O’Brien GD, Bains LM, Simposn J, Collins WP, Campbell S (1980) Ultrasound scanning of ovaries to detect ovulation in women. Fertil Steril 34:99–105PubMedGoogle Scholar
  127. Renaud RL, Macler J, Dervain I, Ehret MC, Aron C, Plas-Roser S, Spira A, Pollack H (1980) Echographic study of follicular maturation and ovulation during the normal menstrual cycle. Fertil Steril 33:272–276PubMedGoogle Scholar
  128. Risch HA, Howe GR (1995) Pelvic inflammatory disease and the risk of epithelial ovarian cancer. Cancer Epidemiol Biomarkers Prev 4:447PubMedGoogle Scholar
  129. Robillard P-Y, Dekker G, Chaouat G, Chaline J, Hulsey T (2008) Possible role of eclampsia/preeclampsia in evolution of human reproduction. In: Trevathan W, Smith E, McKenna J (eds) Evolutionary medicine and health: new perspectives. Oxford University Press, New YorkGoogle Scholar
  130. Rook GAW (2008) The changing microbial environment and chronic inflammatory disorders. Allergy Asthma Clin Immunol 4(3):117–124Google Scholar
  131. Rook GAW (2009) Review series on helminths, immune modulation and the hygiene hypothesis: the broader implications of the hygiene hypothesis. Immunology 126:3–11PubMedGoogle Scholar
  132. Rooks C, Veledar E, Goldberg J, Bremner JD, Vaccarino V (2012) Early trauma and inflammation: role of familial factors in a study of twins. Psychosom Med 74:146–152PubMedGoogle Scholar
  133. Rusterholz C (2007) Role of placentally produced inflammatory and regulatory cytokines in pregnancy and the etiology of preeclampsia. Semin Immunopathol 29:151PubMedGoogle Scholar
  134. Rutherford J, McDade TW, Lee NR, Adair L, Kuzawa C (2009) Change in waist circumference over 11 years and current waist circumference independently predict elevated CRP in Filipino women. Am J Hum Biol 22:310–315Google Scholar
  135. Rutherford J, McDade T, Feranil A, Adair L, Kuzawa C (2010) High prevalence of low HDL-c in the Philippines compared to the US: population differences in associations with diet and BMI. Asia Pac J Clin Nutr 19:57–67PubMedGoogle Scholar
  136. Rutter M, Meigs J, Sullivan L, D’Agostino R Sr, Wilson P (2004) C-reactive protein, the metabolic syndrome, and prediction of cardiovascular events in the Framingham Offspring Study. Circulation 110:380PubMedGoogle Scholar
  137. Sacks GP, Seyani L, Lavery S, Trew G (2004) Maternal C-reactive protein levels are raised at 4 weeks gestation. Hum Reprod 19:1025–1030PubMedGoogle Scholar
  138. Sainz de la Cuesta R, Eichhorn JH, Rice LW, Fuller AF (1996) Histologic transformation of benign endometriosis to early epithelial ovarian cancer. Gynecol Oncol 60:238–244PubMedGoogle Scholar
  139. Salafia CM, Pezzullo JC, López-Zeno J, Simmens S, Minior VK, Vintzileos AM (1995) Placental pathologic features of preterm preeclampsia. Am J Obstet Gynecol 173:1097–1105PubMedGoogle Scholar
  140. Sanders K, Bruce N (1999) Psychosocial stress and the menstrual cycle. J Biosoc Sci 31:393–402PubMedGoogle Scholar
  141. Shibahara H, Suzuki T, Kikuchi K, Hirano Y, Suzuki M (2005) Serum matrix metalloproteinase and tissue inhibitor of metalloproteinase concentrations in infertile women achieved pregnancy following IVF-ET. Am J Reprod Immunol 54:186–192PubMedGoogle Scholar
  142. Slopen N, Lewis TT, Gruenewald TL, Mujahid MS, Ryff CD, Albert MA, Williams DR (2010) Early life adversity and inflammation in African Americans and whites in the midlife in the United States survey. Psychosom Med 72:694PubMedGoogle Scholar
  143. Smith MF, Ricke WA, Bakke LJ, Dow MPD, Smith GW (2002) Ovarian tissue remodeling: role of matrix metalloproteinases and their inhibitors. Mol Cell Endocrinol 191:45–56PubMedGoogle Scholar
  144. Steel DM, Whitehead AS (1994) The major acute phase reactants: C-reactive protein, serum amyloid P component and serum amyloid A protein. Immunol Today 15:81–88PubMedGoogle Scholar
  145. Sterner K, Jameson N, Wildman D (2012) Placental development, evolution, and epigenetics of primate pregnancies. In: Clancy K, Hinde K, Rutherford J (eds) Building babies: primate development in proximate and ultimate perspective. Springer, New York (this volume)Google Scholar
  146. Tanaka Y, Narahara H, Takai N, Yoshimatsu J, Anai T, Miyakawa I (1998) Interleukin-1beta and interleukin-8 in cervicovaginal fluid during pregnancy. Am J Obstet Gynecol 1998 179:644–649PubMedGoogle Scholar
  147. Thurston RC, Kubzansky LD (2007) Multiple sources of psychosocial disadvantage and risk of coronary heart disease. Psychosom Med 69:748–755PubMedGoogle Scholar
  148. Trentham-Dietz A, Nichols HB, Hampton JM, Newcomb PA (2006) Weight change and risk of endometrial cancer. Int J Epidemiol 35:151–158PubMedGoogle Scholar
  149. van Noordwijk MA, van Schaik CP (2005) Development of ecological competence in Sumatran orangutans. Am J Phys Anthropol 127:79–94PubMedGoogle Scholar
  150. Wadhwa P, Culhane J, Rauh V, Barve S (2001) Stress and preterm birth: neuroendocrine, immune/inflammatory, and vascular mechanisms. Matern Child Health J 5:119–125PubMedGoogle Scholar
  151. Walker RS, Gurven M, Burger O, Hamilton MJ (2008) The trade-off between number and size of offspring in humans and other primates. Proc R Soc B Biol Sci 275:827Google Scholar
  152. Wander K, Brindle E, O’Connor KA (2008) C-reactive protein across the menstrual cycle. Am J Phys Anthropol 136:138–146PubMedGoogle Scholar
  153. Watts DP (1991) Mountain gorilla reproduction and sexual behavior. Am J Primatol 24:211–225Google Scholar
  154. Wilcox AJ, Dunson D, Baird DD (2000) The timing of the “fertile window” in the menstrual cycle: day specific estimates from a prospective study. BMJ 321:1259–1262PubMedGoogle Scholar
  155. Williams M, Williams S, Milne B, Hancox R, Poulton R (2004) Association between C-reactive protein, metabolic cardiovascular risk factors, obesity and oral contraceptive use in young adults. Int J Obes 28:998–1003Google Scholar
  156. Wood JW (1994) Dynamics of human reproduction: biology, biometry, demography. Aldine de Gruyter, HawthorneGoogle Scholar
  157. Wu H-M, Wang H-S, Huang H-Y, Soong Y-K, MacCalman CD & Leung PC (2009) GnRH signaling in intrauterine tissues. Reproduction 137:769–777Google Scholar
  158. Wunder DM, Yared M, Bersinger NA, Widmer D, Kretschmer R, Birkhauser MH (2006) Serum leptin and C-reactive protein levels in the physiological spontaneous menstrual cycle in reproductive age women. Eur J Endocrinol 155:137–142PubMedGoogle Scholar
  159. Yoshikawa H, Jimbo H, Okada S, Matsumoto K, Onda T, Yasugi T, Taketani Y (2000) Prevalence of endometriosis in ovarian cancer. Gynecol Obstet Invest 50:11–17PubMedGoogle Scholar
  160. Yudkin JS, Stehouwer CDA, Emeis JJ, Coppack SW (1999) C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue? Arterioscler Thromb Vasc Biol 19:972–978PubMedGoogle Scholar
  161. Zhu J, Quyyumi AA, Norman JE, Csako G, Waclawiw MA, Shearer GM, Epstein SE (2000) Effects of total pathogen burden on coronary artery disease risk and C-reactive protein levels. Am J Cardiol 85:140–146PubMedGoogle Scholar

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© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of Illinois, Urbana-ChampaignUrbanaUSA

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