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Obesity in Pregnancy Stimulates Macrophage Accumulation and Inflammation in the Placenta
Open accessAbstract
Obesity and pregnancy are associated with a combination of insulin resistance and inflammatory changes which exacerbate in combination. Based on the similarity between the inflammatory transcriptomes of adipose tissue and placenta, we hypothesized that the placenta develops exaggerated inflammation in response to obesity. The aim of this study was to characterize placental inflammatory mediators and macrophage accumulation in relation to peripheral inflammation in obesity. Placental macrophages and maternal peripheral blood mononuclear cells (PBMC) from 20 obese and 15 lean women were functionally and phenotypically characterized using immunohistochemistry, flow cytometry and expression for macrophage markers and inflammatory cytokines. The number of resident CD68+ and CD14+ cells was increased 2-3 fold in the placenta of obese as compared to lean women. The macrophage population was characterized by a marked phenotypic heterogeneity with complex subsets of CD14+, CD68+ and CD11b+ (mac-1) cells and by an increased expression of the pro-inflammatory cytokines IL-1, TNF-alpha, IL-6. Placental inflammation was associated with an activation of PBMC gene expression with an increase in the monocyte differentiation and maturation markers CD14 and CD68 in maternal but not fetal PBMC. The inflammatory changes were associated with higher plasma concentrations of C-reactive protein and IL-6 in obese compared to lean women. In conclusion, the chronic inflammation state of pre-gravid obesity is extending to in utero life with accumulation of a heterogeneous macrophage population and pro-inflammatory mediators in the placenta. The resulting inflammatory milieu in which the fetus develops may have critical consequences for short and long term programming of obesity.
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“Increased oxidative stress and inflammation markers have been found in the placenta of obese mothers, suggesting a decisive role of an abnormal intrauterine environment in modulating fetal programming [76,79].”
From Maternal Overnutrition and Fetal Programming: Long-Term Metabolic, Cognitive, and Epigenetic Consequences (2026) · cites this paper as [79]
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“Therefore, fetuses of obese mothers are exposed to an imbalance of cytokines, as well as nutrients that can negatively affect fetal programming, leading to adverse long-term effects in the offspring.”
From Maternal Overnutrition and Fetal Programming: Long-Term Metabolic, Cognitive, and Epigenetic Consequences (2026) · cites this paper as [79]
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“The negative effect of maternal obesity on offspring health might be mediated by an alteration in the inflammatory state and an increase in oxidative stress due to excess adipose tissue.”
From Maternal Overnutrition and Fetal Programming: Long-Term Metabolic, Cognitive, and Epigenetic Consequences (2026) · cites this paper as [79]
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“Pregnancy is normally an inflammatory state caused by the remodeling of immunological system to allow embryo implantation, growth and life, regulated by a delicate balance of pro-inflammatory and anti-inflammatory cytokines; in pregnancies complicated by obesity, this balance is shifted mainly towards a pro-inflammatory state.”
From Maternal Overnutrition and Fetal Programming: Long-Term Metabolic, Cognitive, and Epigenetic Consequences (2026) · cites this paper as [79]
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“Evidence of a key role of inflammation in fetal programming was provided by Reynolds et al. in 2015, thanks to a study where supplementation with an anti-inflammatory molecule, the conjugated linoleic acid, led to a reduction in the expression of pro-inflammatory cytokines such as TNF-α and IL-1β and metabolic dysfunction in offspring [76,79].”
From Maternal Overnutrition and Fetal Programming: Long-Term Metabolic, Cognitive, and Epigenetic Consequences (2026) · cites this paper as [79]
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“A number of maternal conditions, both infectious and non-infectious, have been linked to placental inflammation (102, 453).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [102]
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O’Reilly, J. R., & Reynolds, R. M. (2012) · Clinical Endocrinology · doi:10.1111/cen.12055 · Cited by 285
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ResultMaternal-Fetal Inflammation in the Placenta and the Developmental Origins of Health and Disease
Goldstein, J. A., Gallagher, K., Beck, C., Kumar, R., & Gernand, A. D. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.531543 · Cited by 255
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The Placenta and Gestational Diabetes Mellitus
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“In particular, our data suggest that the increased IL-6 and TNF- levels in pregnant women who are obese or have diabetes (1, 3) may play a role in upregulation of placental system A amino acid transport in these conditions (18, 19), contributing to fetal overgrowth.”
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“Compared to the placentas of their lean peers, the placentas of obese women tend to have increased CD68+ and CD14+ cells, along with increased expression of the proinflammatory cytokines IL-1, TNF-α, IL-6, and C-reactive protein (54).”
Haghiac, M., Yang, X.-H., Presley, L. H., Smith, S., Dettelback, S., Minium, J., Belury, M. A., Catalano, P. M., & Mouzon, S. H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137309 · Cited by 140
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“Several of the cytokines showed expression patterns that have already been described in human term placenta, and the data presented here are consistent with those [25].”
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The consequences of obesity and excess weight gain in pregnancy
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Role of the NLRP3 Inflammasome in Preeclampsia
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Regulation of Placental Amino Acid Transport and Fetal Growth
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Gohir, W., Kennedy, K. M., Wallace, J. G., Saoi, M., Bellissimo, C. J., Britz‐McKibbin, P., Petrik, J., Surette, M. G., & Sloboda, D. M. (2019) · The Journal of Physiology · doi:10.1113/jp277353 · Cited by 133
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“Increased macrophage accumulation and heightened levels of pro-inflammatory cytokines have also been demonstrated in the placenta of pre-gravid obese women compared to lean controls [5].”
BackgroundNousen, E. K., Franco, J. G., & Sullivan, E. L. (2013) · Neuroendocrinology · doi:10.1159/000355632 · Cited by 123
Martino, J., Sebert, S. P., Segura, M. T., Garcia-Valdes, L., Florido, J., Padilla, M. C., Marcos, A., Rueda, R., McArdle, H. J., Budge, H., et al. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2015-2590 · Cited by 124
Persson, M., Johansson, S., Villamor, E., & Cnattingius, S. (2014) · PLoS Medicine · doi:10.1371/journal.pmed.1001648 · Cited by 121
“Obesity is also associated with an increased risk of thrombosis during pregnancy [34] and a state of inflammation in the placenta [35], both of which may reduce placental blood flow.”
BackgroundSchliefsteiner, C., Peinhaupt, M., Kopp, S., Loegl, J., Lang, I., Hiden, U., Heinemann, Á., Desoyé, G., & Wadsack, C. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00888 · Cited by 120
“They found that mRNA levels of IL-6 and TNFα, and also IL-1 were upregulated in obese placentae (60), supporting our findings.”
ResultWesolowski, S. R., Baquero, K. C., Newsom, S. A., Kasmi, K. C. E., Bergman, B. C., Shulman, G. I., Grove, K. L., & Friedman, J. E. (2014) · Diabetes · doi:10.2337/db14-0276 · Cited by 119
Metabolic abnormalities and obesity’s impact on the risk for developing preeclampsia
Spradley, F. T. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00440.2016 · Cited by 118
Ghosh, S., Sinha, J. K., Putcha, U. K., & Raghunath, M. (2016) · Frontiers in Nutrition · doi:10.3389/fnut.2016.00001 · Cited by 117
Zambrano, E., Martínez‐Samayoa, P. M., Rodríguez-González, G. L., & Nathanielsz, P. W. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.190033 · Cited by 117
“Journal compilation C© 2010 The Physiological Society Elmquist et al. 1998; Proulx et al. 2001; Yura et al. 2005; Bautista et al. 2008; Delahaye et al. 2008; Kirk et al. 2009).”
Denizli, M., Capitano, M. L., & Kua, K. L. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.940937 · Cited by 125
“Cord blood and placental tissues collected at delivery also facilitate the understanding of immune adaptations of different compartments (maternal plasma, maternal-fetal interface, fetal plasma) during pregnancy (Challier et al., 2008; Laskewitz et al., 2019; Enninga et al., 2021; Jaramillo-Ospina et al., 2021).”
BackgroundMaternal Obesity Promotes a Proinflammatory Signature in Rat Uterus and Blastocyst
Shankar, K., Zhong, Y., Kang, P., Lau, F., Blackburn, M. L., Chen, J., Borengasser, S. J., Ronis, M. J. J., & Badger, T. M. (2011) · Endocrinology · doi:10.1210/en.2010-1078 · Cited by 115
Monocytes and macrophages in pregnancy: The good, the bad, and the ugly*
True, H., Blanton, M. B., Sureshchandra, S., & Messaoudi, I. (2022) · Immunological Reviews · doi:10.1111/imr.13080 · Cited by 115
Lakshmanan, A., Chiu, Y.-H. M., Coull, B. A., Just, A. C., Maxwell, S. L., Schwartz, J. D., Gryparis, A., Kloog, I., Wright, R. J., & Wright, R. O. (2015) · Environmental Research · doi:10.1016/j.envres.2014.10.035 · Cited by 115
The placenta is the center of the chronic disease universe
Thornburg, K. L. R., & Marshall, N. (2015) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2015.08.030 · Cited by 121
Higgins, L. E., Greenwood, S. L., Wareing, M., Sibley, C. P., & Mills, T. A. (2010) · Placenta · doi:10.1016/j.placenta.2010.09.019 · Cited by 112
“4[[118] 4[ [118] 4[ [32,36,37,79]”
The impact of maternal high-fat diet on offspring neurodevelopment
Urbonaite, G., Knyzeliene, A., Bunn, F. S., Smalskys, A., & Neniškytė, U. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.909762 · Cited by 124
“, 2014) with an expected negative impact on offspring neurodevelopment (Challier et al., 2008; Kim et al., 2014).”
BackgroundHeerwagen, M. J. R., Stewart, M. S., de la Houssaye, B. A., Janssen, R. C., & Friedman, J. E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067791 · Cited by 116
Hastie, R., & Lappas, M. (2014) · Placenta · doi:10.1016/j.placenta.2014.06.368 · Cited by 107
“Although not investigated in the present study, pre-existing maternal obesity has been previously linked to a heightened inflammatory response within placental tissue, with significant increases in pro-inflammatory cytokines such as TNF-a, IL-1b, IL-8 and IL-6 [55,57].”
BackgroundMechanisms by which maternal obesity programs offspring for obesity: evidence from animal studies
Zambrano, E., & Nathanielsz, P. W. (2013) · Nutrition Reviews · doi:10.1111/nure.12068 · Cited by 114
Nogues, P., Santos, E. D., Jammes, H., Berveiller, P., Arnould, L., Vialard, F., & Dieudonné, M. (2019) · Clinical Epigenetics · doi:10.1186/s13148-019-0612-6 · Cited by 114
Effects of Maternal Obesity on Fetal Programming: Molecular ApproachesPreprint
Neri, C., & Edlow, A. G. (2015) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a026591 · Cited by 110
Effect of IL-6 and TNF-α on fatty acid uptake in cultured human primary trophoblast cells
Lager, S., Jansson, N., Olsson, A., Wennergren, M., Jansson, T., & Powell, T. L. (2010) · Placenta · doi:10.1016/j.placenta.2010.10.012 · Cited by 106
“In addition to elevated circulatory lipids, obese and GDM women have increased levels of pro-inflammatory cytokines (interleukin (IL)-6 and tumor necrosis factor (TNF)-a), along with certain hormones, including insulin and leptin [9,10].”
BackgroundFeto-placental Adaptations to Maternal Obesity in the Baboon
Farley, D. R., Tejero, M. E., Comuzzie, A. G., Higgins, P. B., Cox, L. A., Werner, S. L., Jenkins, S. L., Li, C., Choi, J., Dick, E. J., et al. (2009) · Placenta · doi:10.1016/j.placenta.2009.06.007 · Cited by 104
“Maternal obesity in pregnancy is associated with maternal PBMC activation and placental macrophage infiltration [14].”
BackgroundObesity during pregnancy and fetal iron status: is Hepcidin the link?
Dao, M. C., Sen, S., Iyer, C., Klebenov, D., & Meydani, S. N. (2012) · Journal of Perinatology · doi:10.1038/jp.2012.81 · Cited by 107
An evolving scientific basis for the prevention and treatment of pediatric obesity
Katzmarzyk, P. T., Barlow, S. E., Bouchard, C., Catalano, P. M., Hsia, D. S., Inge, T. H., Lovelady, C., Raynor, H. A., Redman, L. M., Staiano, A. E., et al. (2014) · International Journal of Obesity · doi:10.1038/ijo.2014.49 · Cited by 106
Self-citationZambrano, E., Ibáñez, C. A., Martínez‐Samayoa, P. M., Lomas‐Soria, C., Durand-Carbajal, M., & Rodríguez-González, G. L. (2016) · Archives of Medical Research · doi:10.1016/j.arcmed.2016.01.004 · Cited by 107
Jayabalan, N., Nair, S., Nuzhat, Z., Rice, G. E., Zuñiga, F. A., Sobrevía, L., Leiva, A., Sanhueza, C., Gutiérrez, J., Lappas, M., et al. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00239 · Cited by 106
Elfeky, O. W. M., Longo, S. A., Lai, A., Rice, G. E., & Salomón, C. (2016) · Placenta · doi:10.1016/j.placenta.2016.12.020 · Cited by 103
Maternal Low-Grade Chronic Inflammation and Intrauterine Programming of Health and Disease
Parisi, F., Milazzo, R., Savasi, V. M., & Cetin, I. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22041732 · Cited by 117
“As expected, local macrophage infiltration and increased proinflammatory mediators, including IL-6, leptin, and TNF, were shown in obese placentas [27].”
BackgroundVisiedo, F., Bugatto, F., Sánchez-Encinales, V., Cózar‐Castellano, I., Bartha, J. L., & Perdomo, G. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00032.2013 · Cited by 103
“Several studies support the idea that GDM and/or obesity induces inflammatory pathways in placenta (7, 12, 24, 35).”
BackgroundIncreased glucose and placental GLUT-1 in large infants of obese nondiabetic mothers
Acosta, O., Ramirez, V. I., Lager, S., Gaccioli, F., Dudley, D. J., Powell, T. L., & Jansson, T. (2015) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2014.08.009 · Cited by 102
Descriptive epidemiology of idiopathic clubfoot
Werler, M. M., Yazdy, M. M., Mitchell, A. A., Meyer, R. E., Druschel, C. M., Anderka, M., Kasser, J. R., & Mahan, S. T. (2013) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.35955 · Cited by 102
“Vascular inflammation and oxidative stress are linked to obesity [Challier et al., 2008; Farah et al., 2012], which may be exacerbated in the presence of fetal constraint or geneticpredisposing factors or may interfere with recovery from vascular damage.”
BackgroundMaternal obesity and sex-specific differences in placental pathology
Leon-Garcia, S., Roeder, H., Nelson, K. K., Liao, X., Pizzo, D. P., Laurent, L. C., Parast, M. M., & LaCoursiere, D. Y. (2015) · Placenta · doi:10.1016/j.placenta.2015.12.006 · Cited by 100
Metadata
- Authors
- Challier, J. C., Basu, S., Bintein, T., Minium, J., Hotmire, K., Catalano, P. M., & Hauguel-de Mouzon, S.
- Affiliations
- Université Pierre-et-Marie-Curie (FR)
- MetroHealth (US)
- ORCID
- Catalano, P.M.
- Venue
- Placenta
- Publisher
- Elsevier BV
- Published
- 2008-03
- Volume
- 29
- Issue
- 3
- Pages
- 274-281
- ISSN
- 0143-4004 (ISSN-L)
- PMC
- PMC4284075
- OpenAlex
- W1975136933
- Cited by
- 712
- References
- 48
- Citations by year
- 2026: 18 · 2025: 32 · 2024: 25 · 2023: 47 · 2022: 57 · 2021: 30 · 2020: 66 · 2019: 33 · 2018: 44 · 2017: 48 · 2016: 51 · 2015: 67 · 2014: 53 · 2013: 46 · 2012: 34
- FWCI
- 22.63
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Placenta (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Deutsches Krebsforschungszentrum
- National Institutes of Health
- National Center for Research Resources (M01RR000080, RR 00080)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD022965, HD-22965)
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Gestational Diabetes Research and Management
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Keywords
- maternal obesity, placental inflammation, placental macrophages, macrophage heterogeneity, CD68, CD14, CD11b, inflammatory cytokines, interleukin-6, TNF-α, interleukin-1, C-reactive protein, insulin resistance, fetal programming
- MeSH terms
- CD68 Molecule, Adult, Calcium-Binding Proteins, Cell Count, Cells, Cultured, Female, Fetal Blood, Humans, Inflammation, Leukocytes, Mononuclear, Macrophages, Membrane Glycoproteins, Mucins, Obesity, Placenta, Pregnancy, Pregnancy Complications, Tumor Necrosis Factor-alpha, Antigens, Differentiation, Myelomonocytic, Antigens, CD, Interleukin-6, Lipopolysaccharide Receptors, Receptors, G-Protein-Coupled
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